diff --git a/packages/@react-aria/dnd/src/DragManager.ts b/packages/@react-aria/dnd/src/DragManager.ts
index 851466dd273..0e818675496 100644
--- a/packages/@react-aria/dnd/src/DragManager.ts
+++ b/packages/@react-aria/dnd/src/DragManager.ts
@@ -13,7 +13,6 @@
 import {announce} from '@react-aria/live-announcer';
 import {ariaHideOutside} from '@react-aria/overlays';
 import {DragEndEvent, DragItem, DropActivateEvent, DropEnterEvent, DropEvent, DropExitEvent, DropItem, DropOperation, DropTarget as DroppableCollectionTarget, FocusableElement} from '@react-types/shared';
-import {flushSync} from 'react-dom';
 import {getDragModality, getTypes} from './utils';
 import {isVirtualClick, isVirtualPointerEvent} from '@react-aria/utils';
 import type {LocalizedStringFormatter} from '@internationalized/string';
@@ -26,6 +25,7 @@ let subscriptions = new Set<() => void>();
 
 interface DropTarget {
   element: FocusableElement,
+  preventFocusOnDrop?: boolean,
   getDropOperation?: (types: Set<string>, allowedOperations: DropOperation[]) => DropOperation,
   onDropEnter?: (e: DropEnterEvent, dragTarget: DragTarget) => void,
   onDropExit?: (e: DropExitEvent) => void,
@@ -513,19 +513,11 @@ class DragSession {
       });
     }
 
-    // Blur and re-focus the drop target so that the focus ring appears.
-    if (this.currentDropTarget) {
-      // Since we cancel all focus events in drag sessions, refire blur to make sure state gets updated so drag target doesn't think it's still focused
-      // i.e. When you from one list to another during a drag session, we need the blur to fire on the first list after the drag.
-      if (!this.dragTarget.element.contains(this.currentDropTarget.element)) {
-        this.dragTarget.element.dispatchEvent(new FocusEvent('blur'));
-        this.dragTarget.element.dispatchEvent(new FocusEvent('focusout', {bubbles: true}));
-      }
-      // Re-focus the focusedKey upon reorder. This requires a React rerender between blurring and focusing.
-      flushSync(() => {
-        this.currentDropTarget.element.blur();
-      });
-      this.currentDropTarget.element.focus();
+    if (this.currentDropTarget && !this.currentDropTarget.preventFocusOnDrop) {
+      // Re-trigger focus event on active element, since it will not have received it during dragging (see cancelEvent).
+      // This corrects state such as whether focus ring should appear.
+      // useDroppableCollection handles this itself, so this is only for standalone drop zones.
+      document.activeElement.dispatchEvent(new FocusEvent('focusin', {bubbles: true}));
     }
 
     this.setCurrentDropTarget(null);
diff --git a/packages/@react-aria/dnd/src/useDroppableCollection.ts b/packages/@react-aria/dnd/src/useDroppableCollection.ts
index 6a03bd6fad1..3a19b073b75 100644
--- a/packages/@react-aria/dnd/src/useDroppableCollection.ts
+++ b/packages/@react-aria/dnd/src/useDroppableCollection.ts
@@ -57,6 +57,9 @@ interface DroppingState {
   collection: Collection<Node<unknown>>,
   focusedKey: Key,
   selectedKeys: Set<Key>,
+  target: DropTarget,
+  draggingKeys: Set<Key>,
+  isInternal: boolean,
   timeout: ReturnType<typeof setTimeout>
 }
 
@@ -213,26 +216,93 @@ export function useDroppableCollection(props: DroppableCollectionOptions, state:
   });
 
   let droppingState = useRef<DroppingState>(null);
-  let onDrop = useCallback((e: DropEvent, target: DropTarget) => {
+  let updateFocusAfterDrop = useCallback(() => {
     let {state} = localState;
+    if (droppingState.current) {
+      let {
+        target,
+        collection: prevCollection,
+        selectedKeys: prevSelectedKeys,
+        focusedKey: prevFocusedKey,
+        isInternal,
+        draggingKeys
+      } = droppingState.current;
+      
+      // If an insert occurs during a drop, we want to immediately select these items to give
+      // feedback to the user that a drop occurred. Only do this if the selection didn't change
+      // since the drop started so we don't override if the user or application did something.
+      if (
+        state.collection.size > prevCollection.size &&
+        state.selectionManager.isSelectionEqual(prevSelectedKeys)
+      ) {
+        let newKeys = new Set<Key>();
+        for (let key of state.collection.getKeys()) {
+          if (!prevCollection.getItem(key)) {
+            newKeys.add(key);
+          }
+        }
 
-    // Focus the collection.
-    state.selectionManager.setFocused(true);
+        state.selectionManager.setSelectedKeys(newKeys);
 
-    // Save some state of the collection/selection before the drop occurs so we can compare later.
-    let focusedKey = state.selectionManager.focusedKey;
+        // If the focused item didn't change since the drop occurred, also focus the first
+        // inserted item. If selection is disabled, then also show the focus ring so there
+        // is some indication that items were added.
+        if (state.selectionManager.focusedKey === prevFocusedKey) {
+          let first = newKeys.keys().next().value;
+          let item = state.collection.getItem(first);
+
+          // If this is a cell, focus the parent row.
+          if (item?.type === 'cell') {
+            first = item.parentKey;
+          }
+
+          state.selectionManager.setFocusedKey(first);
 
-    // If parent key was dragged, we want to use it instead (i.e. focus row instead of cell after dropping)
-    if (globalDndState.draggingKeys.has(state.collection.getItem(focusedKey)?.parentKey)) {
-      focusedKey = state.collection.getItem(focusedKey).parentKey;
-      state.selectionManager.setFocusedKey(focusedKey);
+          if (state.selectionManager.selectionMode === 'none') {
+            setInteractionModality('keyboard');
+          }
+        }
+      } else if (
+        state.selectionManager.focusedKey === prevFocusedKey &&
+        isInternal &&
+        target.type === 'item' &&
+        target.dropPosition !== 'on' &&
+        draggingKeys.has(state.collection.getItem(prevFocusedKey)?.parentKey)
+      ) {
+        // Focus row instead of cell when reordering.
+        state.selectionManager.setFocusedKey(state.collection.getItem(prevFocusedKey).parentKey);
+        setInteractionModality('keyboard');
+      } else if (
+        state.selectionManager.focusedKey === prevFocusedKey &&
+        target.type === 'item' && 
+        target.dropPosition === 'on' && 
+        state.collection.getItem(target.key) != null
+      ) {
+        // If focus didn't move already (e.g. due to an insert), and the user dropped on an item,
+        // focus that item and show the focus ring to give the user feedback that the drop occurred.
+        // Also show the focus ring if the focused key is not selected, e.g. in case of a reorder.
+        state.selectionManager.setFocusedKey(target.key);
+        setInteractionModality('keyboard');
+      } else if (!state.selectionManager.isSelected(state.selectionManager.focusedKey)) {
+        setInteractionModality('keyboard');
+      }
+
+      state.selectionManager.setFocused(true);
     }
+  }, [localState]);
 
+  let onDrop = useCallback((e: DropEvent, target: DropTarget) => {
+    let {state} = localState;
+    
+    // Save some state of the collection/selection before the drop occurs so we can compare later.
     droppingState.current = {
       timeout: null,
-      focusedKey,
+      focusedKey: state.selectionManager.focusedKey,
       collection: state.collection,
-      selectedKeys: state.selectionManager.selectedKeys
+      selectedKeys: state.selectionManager.selectedKeys,
+      draggingKeys: globalDndState.draggingKeys,
+      isInternal: isInternalDropOperation(ref),
+      target
     };
 
     let onDropFn = localState.props.onDrop || defaultOnDrop;
@@ -246,26 +316,13 @@ export function useDroppableCollection(props: DroppableCollectionOptions, state:
     });
 
     // Wait for a short time period after the onDrop is called to allow the data to be read asynchronously
-    // and for React to re-render. If an insert occurs during this time, it will be selected/focused below.
-    // If items are not "immediately" inserted by the onDrop handler, the application will need to handle
-    // selecting and focusing those items themselves.
+    // and for React to re-render. If the collection didn't already change during this time (handled below),
+    // update the focused key here.
     droppingState.current.timeout = setTimeout(() => {
-      // If focus didn't move already (e.g. due to an insert), and the user dropped on an item,
-      // focus that item and show the focus ring to give the user feedback that the drop occurred.
-      // Also show the focus ring if the focused key is not selected, e.g. in case of a reorder.
-      let {state} = localState;
-
-      if (target.type === 'item' && target.dropPosition === 'on' && state.collection.getItem(target.key) != null) {
-        state.selectionManager.setFocusedKey(target.key);
-        state.selectionManager.setFocused(true);
-        setInteractionModality('keyboard');
-      } else if (!state.selectionManager.isSelected(focusedKey)) {
-        setInteractionModality('keyboard');
-      }
-
+      updateFocusAfterDrop();
       droppingState.current = null;
     }, 50);
-  }, [localState, defaultOnDrop]);
+  }, [localState, defaultOnDrop, ref, updateFocusAfterDrop]);
 
   // eslint-disable-next-line arrow-body-style
   useEffect(() => {
@@ -277,44 +334,9 @@ export function useDroppableCollection(props: DroppableCollectionOptions, state:
   }, []);
 
   useLayoutEffect(() => {
-    // If an insert occurs during a drop, we want to immediately select these items to give
-    // feedback to the user that a drop occurred. Only do this if the selection didn't change
-    // since the drop started so we don't override if the user or application did something.
-    if (
-      droppingState.current &&
-      state.selectionManager.isFocused &&
-      state.collection.size > droppingState.current.collection.size &&
-      state.selectionManager.isSelectionEqual(droppingState.current.selectedKeys)
-    ) {
-      let newKeys = new Set<Key>();
-      for (let key of state.collection.getKeys()) {
-        if (!droppingState.current.collection.getItem(key)) {
-          newKeys.add(key);
-        }
-      }
-
-      state.selectionManager.setSelectedKeys(newKeys);
-
-      // If the focused item didn't change since the drop occurred, also focus the first
-      // inserted item. If selection is disabled, then also show the focus ring so there
-      // is some indication that items were added.
-      if (state.selectionManager.focusedKey === droppingState.current.focusedKey) {
-        let first = newKeys.keys().next().value;
-        let item = state.collection.getItem(first);
-
-        // If this is a cell, focus the parent row.
-        if (item?.type === 'cell') {
-          first = item.parentKey;
-        }
-
-        state.selectionManager.setFocusedKey(first);
-
-        if (state.selectionManager.selectionMode === 'none') {
-          setInteractionModality('keyboard');
-        }
-      }
-
-      droppingState.current = null;
+    // If the collection changed after a drop, update the focused key.
+    if (droppingState.current && state.collection !== droppingState.current.collection) {
+      updateFocusAfterDrop();
     }
   });
 
@@ -470,6 +492,7 @@ export function useDroppableCollection(props: DroppableCollectionOptions, state:
 
     return DragManager.registerDropTarget({
       element: ref.current,
+      preventFocusOnDrop: true,
       getDropOperation(types, allowedOperations) {
         if (localState.state.target) {
           let {draggingKeys} = globalDndState;
diff --git a/packages/@react-aria/dnd/stories/DraggableCollection.tsx b/packages/@react-aria/dnd/stories/DraggableCollection.tsx
index 8476f15814d..8f871d81a36 100644
--- a/packages/@react-aria/dnd/stories/DraggableCollection.tsx
+++ b/packages/@react-aria/dnd/stories/DraggableCollection.tsx
@@ -58,7 +58,7 @@ function DraggableCollection(props) {
   let state = useListState(props);
   let gridState = useGridState({
     selectionMode: 'multiple',
-    collection: new GridCollection({
+    collection: React.useMemo(() => new GridCollection({
       columnCount: 1,
       items: [...state.collection].map(item => ({
         ...item,
@@ -74,7 +74,7 @@ function DraggableCollection(props) {
           childNodes: []
         }]
       }))
-    })
+    }), [state.collection])
   });
 
   let preview = useRef(null);
diff --git a/packages/@react-aria/dnd/stories/DroppableGrid.tsx b/packages/@react-aria/dnd/stories/DroppableGrid.tsx
index 17c7edbedf6..68f23dfd195 100644
--- a/packages/@react-aria/dnd/stories/DroppableGrid.tsx
+++ b/packages/@react-aria/dnd/stories/DroppableGrid.tsx
@@ -122,7 +122,7 @@ const DroppableGrid = React.forwardRef(function (props: any, ref) {
     focusMode: 'cell',
     selectedKeys: props.selectedKeys,
     onSelectionChange: props.onSelectionChange,
-    collection: new GridCollection({
+    collection: React.useMemo(() => new GridCollection({
       columnCount: 1,
       items: [...state.collection].map(item => ({
         ...item,
@@ -138,7 +138,7 @@ const DroppableGrid = React.forwardRef(function (props: any, ref) {
           childNodes: []
         }]
       }))
-    })
+    }), [state.collection])
   });
 
   React.useImperativeHandle(ref, () => ({
diff --git a/packages/@react-aria/dnd/stories/Reorderable.tsx b/packages/@react-aria/dnd/stories/Reorderable.tsx
index ee09cb6b8c9..564995bde88 100644
--- a/packages/@react-aria/dnd/stories/Reorderable.tsx
+++ b/packages/@react-aria/dnd/stories/Reorderable.tsx
@@ -71,7 +71,7 @@ function ReorderableGrid(props) {
   let keyboardDelegate = new ListKeyboardDelegate(state.collection, new Set(), ref);
   let gridState = useGridState({
     selectionMode: 'multiple',
-    collection: new GridCollection({
+    collection: React.useMemo(() => new GridCollection({
       columnCount: 1,
       items: [...state.collection].map(item => ({
         ...item,
@@ -87,7 +87,7 @@ function ReorderableGrid(props) {
           childNodes: []
         }]
       }))
-    })
+    }), [state.collection])
   });
 
   // Use a random drag type so the items can only be reordered within this list and not dragged elsewhere.
diff --git a/packages/@react-aria/dnd/stories/VirtualizedListBox.tsx b/packages/@react-aria/dnd/stories/VirtualizedListBox.tsx
index d0bc2c9687a..9fefd5ce50c 100644
--- a/packages/@react-aria/dnd/stories/VirtualizedListBox.tsx
+++ b/packages/@react-aria/dnd/stories/VirtualizedListBox.tsx
@@ -21,7 +21,7 @@ import Folder from '@spectrum-icons/workflow/Folder';
 import {Item} from '@react-stately/collections';
 import {ListKeyboardDelegate} from '@react-aria/selection';
 import {ListLayout} from '@react-stately/layout';
-import React from 'react';
+import React, {useMemo} from 'react';
 import {useDropIndicator, useDroppableCollection, useDroppableItem} from '..';
 import {useDroppableCollectionState} from '@react-stately/dnd';
 import {useListBox, useOption} from '@react-aria/listbox';
@@ -159,6 +159,8 @@ export const VirtualizedListBox = React.forwardRef(function (props: any, ref) {
     isVirtualized: true
   }, state, domRef);
   let isDropTarget = dropState.isDropTarget({type: 'root'});
+  let focusedKey = dropState.target?.type === 'item' ? dropState.target.key : state.selectionManager.focusedKey;
+  let persistedKeys = useMemo(() => focusedKey != null ? new Set([focusedKey]) : null, [focusedKey]);
 
   return (
     <Context.Provider value={{state, dropState}}>
@@ -170,7 +172,7 @@ export const VirtualizedListBox = React.forwardRef(function (props: any, ref) {
         scrollDirection="vertical"
         layout={layout}
         collection={state.collection}
-        focusedKey={dropState.target?.type === 'item' ? dropState.target.key : state.selectionManager.focusedKey}>
+        persistedKeys={persistedKeys}>
         {(type, item) => (
           <>
             {state.collection.getKeyBefore(item.key) == null &&
diff --git a/packages/@react-aria/dnd/stories/dnd.stories.tsx b/packages/@react-aria/dnd/stories/dnd.stories.tsx
index 20d26c103c8..f89e66225b6 100644
--- a/packages/@react-aria/dnd/stories/dnd.stories.tsx
+++ b/packages/@react-aria/dnd/stories/dnd.stories.tsx
@@ -386,7 +386,7 @@ function DraggableCollection(props) {
   let gridState = useGridState({
     ...props,
     selectionMode: 'multiple',
-    collection: new GridCollection({
+    collection: React.useMemo(() => new GridCollection({
       columnCount: 1,
       items: [...state.collection].map(item => ({
         ...item,
@@ -402,7 +402,7 @@ function DraggableCollection(props) {
           childNodes: []
         }]
       }))
-    })
+    }), [state.collection])
   });
 
   let preview = useRef(null);
diff --git a/packages/@react-aria/grid/stories/example.tsx b/packages/@react-aria/grid/stories/example.tsx
index c7603f31512..e1e84ed3e9a 100644
--- a/packages/@react-aria/grid/stories/example.tsx
+++ b/packages/@react-aria/grid/stories/example.tsx
@@ -11,7 +11,7 @@ export function Grid(props) {
   let gridState = useGridState({
     ...props,
     selectionMode: 'multiple',
-    collection: new GridCollection({
+    collection: React.useMemo(() => new GridCollection({
       columnCount: 1,
       items: [...state.collection].map(item => ({
         type: 'item',
@@ -21,7 +21,7 @@ export function Grid(props) {
           type: 'cell'
         }]
       }))
-    })
+    }), [state.collection])
   });
 
   let ref = React.useRef(undefined);
diff --git a/packages/@react-aria/virtualizer/src/Virtualizer.tsx b/packages/@react-aria/virtualizer/src/Virtualizer.tsx
index a08ae1a08d4..e098a0ed1ac 100644
--- a/packages/@react-aria/virtualizer/src/Virtualizer.tsx
+++ b/packages/@react-aria/virtualizer/src/Virtualizer.tsx
@@ -13,7 +13,7 @@
 import {Collection, Key} from '@react-types/shared';
 import {Layout, Rect, ReusableView, useVirtualizerState, VirtualizerState} from '@react-stately/virtualizer';
 import {mergeProps, useLayoutEffect} from '@react-aria/utils';
-import React, {HTMLAttributes, ReactElement, ReactNode, RefObject, useCallback, useMemo, useRef} from 'react';
+import React, {HTMLAttributes, ReactElement, ReactNode, RefObject, useCallback, useRef} from 'react';
 import {ScrollView} from './ScrollView';
 import {VirtualizerItem} from './VirtualizerItem';
 
@@ -29,7 +29,7 @@ interface VirtualizerProps<T extends object, V, O> extends Omit<HTMLAttributes<H
   renderWrapper?: RenderWrapper<T, V>,
   layout: Layout<T, O>,
   collection: Collection<T>,
-  focusedKey?: Key,
+  persistedKeys?: Set<Key> | null,
   sizeToFit?: 'width' | 'height',
   scrollDirection?: 'horizontal' | 'vertical' | 'both',
   isLoading?: boolean,
@@ -49,7 +49,7 @@ function Virtualizer<T extends object, V extends ReactNode, O>(props: Virtualize
     isLoading,
     // eslint-disable-next-line @typescript-eslint/no-unused-vars
     onLoadMore,
-    focusedKey,
+    persistedKeys,
     layoutOptions,
     ...otherProps
   } = props;
@@ -65,7 +65,7 @@ function Virtualizer<T extends object, V extends ReactNode, O>(props: Virtualize
       ref.current.scrollLeft = rect.x;
       ref.current.scrollTop = rect.y;
     },
-    persistedKeys: useMemo(() => focusedKey != null ? new Set([focusedKey]) : new Set(), [focusedKey]),
+    persistedKeys,
     layoutOptions
   });
 
diff --git a/packages/@react-spectrum/card/src/BaseLayout.tsx b/packages/@react-spectrum/card/src/BaseLayout.tsx
index a2bc1a0c11b..f62c7fc9a4c 100644
--- a/packages/@react-spectrum/card/src/BaseLayout.tsx
+++ b/packages/@react-spectrum/card/src/BaseLayout.tsx
@@ -53,7 +53,7 @@ export class BaseLayout<T> extends Layout<Node<T>, CardViewLayoutOptions> implem
     this.margin = options.margin || 24;
   }
 
-  validate(invalidationContext: InvalidationContext<CardViewLayoutOptions>) {
+  update(invalidationContext: InvalidationContext<CardViewLayoutOptions>) {
     this.collection = this.virtualizer.collection as GridCollection<T>;
     this.isLoading = invalidationContext.layoutOptions?.isLoading || false;
     this.direction = invalidationContext.layoutOptions?.direction || 'ltr';
diff --git a/packages/@react-spectrum/card/src/CardView.tsx b/packages/@react-spectrum/card/src/CardView.tsx
index 8b166fa2397..97341ade178 100644
--- a/packages/@react-spectrum/card/src/CardView.tsx
+++ b/packages/@react-spectrum/card/src/CardView.tsx
@@ -102,6 +102,8 @@ function CardView<T extends object>(props: SpectrumCardViewProps<T>, ref: DOMRef
     focusedKey = focusedItem.parentKey;
   }
 
+  let persistedKeys = useMemo(() => focusedKey != null ? new Set([focusedKey]) : null, [focusedKey]);
+
   // TODO: does aria-row count and aria-col count need to be modified? Perhaps aria-col count needs to be omitted
   return (
     <CardViewContext.Provider value={{state, isQuiet, layout: cardViewLayout, cardOrientation, renderEmptyState}}>
@@ -110,7 +112,7 @@ function CardView<T extends object>(props: SpectrumCardViewProps<T>, ref: DOMRef
         {...styleProps}
         className={classNames(styles, 'spectrum-CardView')}
         ref={domRef}
-        focusedKey={focusedKey}
+        persistedKeys={persistedKeys}
         scrollDirection="vertical"
         layout={cardViewLayout}
         collection={gridCollection}
diff --git a/packages/@react-spectrum/list/src/ListView.tsx b/packages/@react-spectrum/list/src/ListView.tsx
index a776c299e7f..e9aa0040cb1 100644
--- a/packages/@react-spectrum/list/src/ListView.tsx
+++ b/packages/@react-spectrum/list/src/ListView.tsx
@@ -184,10 +184,19 @@ function ListView<T extends object>(props: SpectrumListViewProps<T>, ref: DOMRef
   }, state, domRef);
 
   let focusedKey = selectionManager.focusedKey;
+  let dropTargetKey: Key | null = null;
   if (dropState?.target?.type === 'item') {
-    focusedKey = dropState.target.key;
+    dropTargetKey = dropState.target.key;
+    if (dropState.target.dropPosition === 'after') {
+      // Normalize to the "before" drop position since we only render those in the DOM.
+      dropTargetKey = state.collection.getKeyAfter(dropTargetKey) ?? dropTargetKey;
+    }
   }
 
+  let persistedKeys = useMemo(() => {
+    return new Set([focusedKey, dropTargetKey].filter(k => k !== null));
+  }, [focusedKey, dropTargetKey]);
+
   // wait for layout to get accurate measurements
   let [isVerticalScrollbarVisible, setVerticalScollbarVisible] = useState(false);
   let [isHorizontalScrollbarVisible, setHorizontalScollbarVisible] = useState(false);
@@ -214,7 +223,7 @@ function ListView<T extends object>(props: SpectrumListViewProps<T>, ref: DOMRef
             isLoading={isLoading}
             onLoadMore={onLoadMore}
             ref={domRef}
-            focusedKey={focusedKey}
+            persistedKeys={persistedKeys}
             scrollDirection="vertical"
             className={
               classNames(
diff --git a/packages/@react-spectrum/list/src/ListViewLayout.ts b/packages/@react-spectrum/list/src/ListViewLayout.ts
index 2044b803bd6..8f8d251eefb 100644
--- a/packages/@react-spectrum/list/src/ListViewLayout.ts
+++ b/packages/@react-spectrum/list/src/ListViewLayout.ts
@@ -20,9 +20,9 @@ interface ListViewLayoutProps {
 export class ListViewLayout<T> extends ListLayout<T, ListViewLayoutProps> {
   private isLoading: boolean = false;
 
-  validate(invalidationContext: InvalidationContext<ListViewLayoutProps>): void {
+  update(invalidationContext: InvalidationContext<ListViewLayoutProps>): void {
     this.isLoading = invalidationContext.layoutOptions?.isLoading || false;
-    super.validate(invalidationContext);
+    super.update(invalidationContext);
   }
 
   protected buildCollection(): LayoutNode[] {
diff --git a/packages/@react-spectrum/list/stories/ListViewDnD.stories.tsx b/packages/@react-spectrum/list/stories/ListViewDnD.stories.tsx
index 87ae808d981..632d02b0f78 100644
--- a/packages/@react-spectrum/list/stories/ListViewDnD.stories.tsx
+++ b/packages/@react-spectrum/list/stories/ListViewDnD.stories.tsx
@@ -111,6 +111,20 @@ export const DragWithinScroll: ListViewStory = {
   name: 'Drag within list scrolling (Reorder)'
 };
 
+let manyItems = [];
+for (let i = 0; i < 100; i++) {
+  manyItems.push({id: 'item' + i, type: 'item', textValue: 'Item ' + i});
+}
+
+export const DragWithinMany: ListViewStory = {
+  render: (args) => (
+    <Flex direction="row" wrap alignItems="center" height={400}>
+      <ReorderExample {...args} items={manyItems} getAllowedDropOperationsAction={getAllowedDropOperationsAction} disabledKeys={['1']} onDrop={action('drop')} onDragStart={action('dragStart')} onDragEnd={action('dragEnd')} />
+    </Flex>
+  ),
+  name: 'Drag within list with many items'
+};
+
 export const DragIntoFolder: ListViewStory = {
   render: (args) => (
     <Flex direction="row" wrap alignItems="center">
diff --git a/packages/@react-spectrum/list/stories/ListViewDnDExamples.tsx b/packages/@react-spectrum/list/stories/ListViewDnDExamples.tsx
index 2b6d2a54f07..a23a3c81df4 100644
--- a/packages/@react-spectrum/list/stories/ListViewDnDExamples.tsx
+++ b/packages/@react-spectrum/list/stories/ListViewDnDExamples.tsx
@@ -85,9 +85,9 @@ let itemList2 = [
 ];
 
 export function ReorderExample(props) {
-  let {onDrop, onDragStart, onDragEnd, disabledKeys = ['2'], ...otherprops} = props;
+  let {items, onDrop, onDragStart, onDragEnd, disabledKeys = ['2'], ...otherprops} = props;
   let list = useListData({
-    initialItems: props.items || itemList1
+    initialItems: items || itemList1
   });
 
   // Use a random drag type so the items can only be reordered within this list and not dragged elsewhere.
diff --git a/packages/@react-spectrum/list/stories/ListViewDnDUtil.stories.tsx b/packages/@react-spectrum/list/stories/ListViewDnDUtil.stories.tsx
index 86e75233219..6da108bb537 100644
--- a/packages/@react-spectrum/list/stories/ListViewDnDUtil.stories.tsx
+++ b/packages/@react-spectrum/list/stories/ListViewDnDUtil.stories.tsx
@@ -74,6 +74,18 @@ export const DragWithin: ListViewStory = {
   name: 'Drag within list (Reorder}'
 };
 
+let manyItems = [];
+for (let i = 0; i < 100; i++) {
+  manyItems.push({identifier: 'item' + i, type: 'item', name: 'Item ' + i});
+}
+
+export const DragWithinMany: ListViewStory = {
+  render: (args) => (
+    <ReorderExampleUtilHandlers {...args} items={manyItems} listViewProps={{overflowMode: 'wrap', height: 400}} />
+  ),
+  name: 'Drag within list with many items'
+};
+
 export const DropOntoItem: ListViewStory = {
   render: (args) => (
     <ItemDropExampleUtilHandlers listViewProps={args} dndOptions={{onDragStart: action('dragStart'), onDragEnd: action('dragEnd')}} />
diff --git a/packages/@react-spectrum/list/stories/ListViewDnDUtilExamples.tsx b/packages/@react-spectrum/list/stories/ListViewDnDUtilExamples.tsx
index 6427ac8aa87..0ecf61a4c33 100644
--- a/packages/@react-spectrum/list/stories/ListViewDnDUtilExamples.tsx
+++ b/packages/@react-spectrum/list/stories/ListViewDnDUtilExamples.tsx
@@ -93,9 +93,9 @@ export function DragExampleUtilHandlers(props) {
 }
 
 export function ReorderExampleUtilHandlers(props) {
-  let {listViewProps, dndOptions} = props;
+  let {listViewProps, dndOptions, items} = props;
   let list = useListData({
-    initialItems: folderList1,
+    initialItems: (items as typeof folderList1) || folderList1,
     getKey: (item) => item.identifier
   });
 
diff --git a/packages/@react-spectrum/listbox/src/ListBoxBase.tsx b/packages/@react-spectrum/listbox/src/ListBoxBase.tsx
index b89ecb13b8f..3b32b9e3450 100644
--- a/packages/@react-spectrum/listbox/src/ListBoxBase.tsx
+++ b/packages/@react-spectrum/listbox/src/ListBoxBase.tsx
@@ -100,6 +100,9 @@ function ListBoxBase<T>(props: ListBoxBaseProps<T>, ref: RefObject<HTMLDivElemen
     );
   }, []);
 
+  let focusedKey = state.selectionManager.focusedKey;
+  let persistedKeys = useMemo(() => focusedKey != null ? new Set([focusedKey]) : null, [focusedKey]);
+
   return (
     <ListBoxContext.Provider value={{state, renderEmptyState, shouldFocusOnHover, shouldUseVirtualFocus}}>
       <FocusScope>
@@ -107,7 +110,7 @@ function ListBoxBase<T>(props: ListBoxBaseProps<T>, ref: RefObject<HTMLDivElemen
           {...styleProps}
           {...mergeProps(listBoxProps, domProps)}
           ref={ref}
-          focusedKey={state.selectionManager.focusedKey}
+          persistedKeys={persistedKeys}
           autoFocus={!!props.autoFocus || undefined}
           sizeToFit="height"
           scrollDirection="vertical"
diff --git a/packages/@react-spectrum/listbox/src/ListBoxLayout.ts b/packages/@react-spectrum/listbox/src/ListBoxLayout.ts
index 6764b869b77..8f9652c4ea4 100644
--- a/packages/@react-spectrum/listbox/src/ListBoxLayout.ts
+++ b/packages/@react-spectrum/listbox/src/ListBoxLayout.ts
@@ -22,9 +22,9 @@ export class ListBoxLayout<T> extends ListLayout<T, ListBoxLayoutProps> {
     this.padding = opts.padding;
   }
 
-  validate(invalidationContext: InvalidationContext<ListBoxLayoutProps>): void {
+  update(invalidationContext: InvalidationContext<ListBoxLayoutProps>): void {
     this.isLoading = invalidationContext.layoutOptions?.isLoading || false;
-    super.validate(invalidationContext);
+    super.update(invalidationContext);
   }
 
   protected buildCollection(): LayoutNode[] {
diff --git a/packages/@react-spectrum/table/src/TableViewBase.tsx b/packages/@react-spectrum/table/src/TableViewBase.tsx
index 0e4de9e3eaa..86e2da13a96 100644
--- a/packages/@react-spectrum/table/src/TableViewBase.tsx
+++ b/packages/@react-spectrum/table/src/TableViewBase.tsx
@@ -404,10 +404,20 @@ function TableViewBase<T extends object>(props: TableBaseProps<T>, ref: DOMRef<H
   }, [propsOnResizeEnd, setIsInResizeMode, setIsResizing]);
 
   let focusedKey = state.selectionManager.focusedKey;
+  let dropTargetKey: Key | null = null;
   if (dropState?.target?.type === 'item') {
-    focusedKey = dropState.target.key;
+    dropTargetKey = dropState.target.key;
+    if (dropState.target.dropPosition === 'before' && dropTargetKey !== state.collection.getFirstKey()) {
+      // Normalize to the "after" drop position since we only render those in the DOM.
+      // The exception to this is for the first row in the table, where we also render the "before" position.
+      dropTargetKey = state.collection.getKeyBefore(dropTargetKey);
+    }
   }
 
+  let persistedKeys = useMemo(() => {
+    return new Set([focusedKey, dropTargetKey].filter(k => k !== null));
+  }, [focusedKey, dropTargetKey]);
+
   let mergedProps = mergeProps(
     isTableDroppable && droppableCollection?.collectionProps,
     gridProps,
@@ -462,7 +472,7 @@ function TableViewBase<T extends object>(props: TableBaseProps<T>, ref: DOMRef<H
         tableState={state}
         layout={layout}
         collection={state.collection}
-        focusedKey={focusedKey}
+        persistedKeys={persistedKeys}
         renderView={renderView}
         renderWrapper={renderWrapper}
         onVisibleRectChange={onVisibleRectChange}
@@ -494,7 +504,7 @@ interface TableVirtualizerProps<T> extends HTMLAttributes<HTMLElement> {
   tableState: TableState<T>,
   layout: TableViewLayout<T>,
   collection: TableCollection<T>,
-  focusedKey: Key | null,
+  persistedKeys: Set<Key> | null,
   renderView: (type: string, content: GridNode<T>) => ReactElement,
   renderWrapper?: (
     parent: View | null,
@@ -513,7 +523,7 @@ interface TableVirtualizerProps<T> extends HTMLAttributes<HTMLElement> {
 
 // This is a custom Virtualizer that also has a header that syncs its scroll position with the body.
 function TableVirtualizer<T>(props: TableVirtualizerProps<T>) {
-  let {tableState, layout, collection, focusedKey, renderView, renderWrapper, domRef, bodyRef, headerRef, onVisibleRectChange: onVisibleRectChangeProp, isFocusVisible, isVirtualDragging, isRootDropTarget, ...otherProps} = props;
+  let {tableState, layout, collection, persistedKeys, renderView, renderWrapper, domRef, bodyRef, headerRef, onVisibleRectChange: onVisibleRectChangeProp, isFocusVisible, isVirtualDragging, isRootDropTarget, ...otherProps} = props;
   let {direction} = useLocale();
   let loadingState = collection.body.props.loadingState;
   let isLoading = loadingState === 'loading' || loadingState === 'loadingMore';
@@ -558,7 +568,7 @@ function TableVirtualizer<T>(props: TableVirtualizerProps<T>) {
       bodyRef.current.scrollTop = rect.y;
       setScrollLeft(bodyRef.current, direction, rect.x);
     },
-    persistedKeys: useMemo(() => focusedKey ? new Set([focusedKey]) : new Set(), [focusedKey]),
+    persistedKeys,
     layoutOptions: useMemo(() => ({
       columnWidths: columnResizeState.columnWidths
     }), [columnResizeState.columnWidths])
@@ -566,10 +576,10 @@ function TableVirtualizer<T>(props: TableVirtualizerProps<T>) {
 
   let memoedVirtualizerProps = useMemo(() => ({
     tabIndex: otherProps.tabIndex,
-    focusedKey,
+    persistedKeys,
     isLoading,
     onLoadMore
-  }), [otherProps.tabIndex, focusedKey, isLoading, onLoadMore]);
+  }), [otherProps.tabIndex, persistedKeys, isLoading, onLoadMore]);
 
   let {virtualizerProps, scrollViewProps: {onVisibleRectChange}} = useVirtualizer(memoedVirtualizerProps, state, domRef);
   let onVisibleRectChangeMemo = useCallback(rect => {
diff --git a/packages/@react-spectrum/table/src/TableViewLayout.ts b/packages/@react-spectrum/table/src/TableViewLayout.ts
index 365bb65b763..483d39a0b42 100644
--- a/packages/@react-spectrum/table/src/TableViewLayout.ts
+++ b/packages/@react-spectrum/table/src/TableViewLayout.ts
@@ -36,7 +36,7 @@ export class TableViewLayout<T> extends TableLayout<T> {
 
     if (this.isLoading) {
       // Add some margin around the loader to ensure that scrollbars don't flicker in and out.
-      let rect = new Rect(40, 40, (width || this.virtualizer.visibleRect.width) - 80, children.length === 0 ? this.virtualizer.visibleRect.height - 80 : 60);
+      let rect = new Rect(40, Math.max(layoutInfo.rect.maxY, 40), (width || this.virtualizer.visibleRect.width) - 80, children.length === 0 ? this.virtualizer.visibleRect.height - 80 : 60);
       let loader = new LayoutInfo('loader', 'loader', rect);
       loader.parentKey = layoutInfo.key;
       loader.isSticky = children.length === 0;
diff --git a/packages/@react-spectrum/table/stories/TableDnD.stories.tsx b/packages/@react-spectrum/table/stories/TableDnD.stories.tsx
index 3f006d7d7cf..4ff47820ac7 100644
--- a/packages/@react-spectrum/table/stories/TableDnD.stories.tsx
+++ b/packages/@react-spectrum/table/stories/TableDnD.stories.tsx
@@ -14,7 +14,7 @@ import {action} from '@storybook/addon-actions';
 import {ComponentMeta} from '@storybook/react';
 import defaultConfig, {TableStory} from './Table.stories';
 import {Divider} from '@react-spectrum/divider';
-import {DragBetweenTablesExample, DragBetweenTablesRootOnlyExample, DragExample, DragOntoRowExample, DragWithoutRowHeaderExample, ReorderExample} from './TableDnDExamples';
+import {DragBetweenTablesExample, DragBetweenTablesRootOnlyExample, DragExample, DragOntoRowExample, DragWithoutRowHeaderExample, items, ReorderExample} from './TableDnDExamples';
 import {Droppable} from '../../../@react-aria/dnd/stories/dnd.stories';
 import {Flex} from '@react-spectrum/layout';
 import React from 'react';
@@ -91,6 +91,23 @@ export const DragWithinTable: TableStory = {
   name: 'Drag within table (Reorder)'
 };
 
+let manyItems = [];
+for (let i = 0; i < 100; i++) {
+  manyItems.push({...items[i % 10], id: `${i}`});
+}
+
+export const DragWithinTableManyItems: TableStory = {
+  args: {
+    disabledKeys: ['Foo 2']
+  },
+  render: (args) => (
+    <Flex direction="row" wrap alignItems="center">
+      <ReorderExample items={manyItems} tableViewProps={args} onDrop={action('drop')} onDragStart={action('dragStart')} onDragEnd={action('dragEnd')} />
+    </Flex>
+  ),
+  name: 'Drag within table many items'
+};
+
 export const DragOntoRow: TableStory = {
   args: {
     disabledKeys: ['1']
diff --git a/packages/@react-spectrum/table/stories/TableDnDExamples.tsx b/packages/@react-spectrum/table/stories/TableDnDExamples.tsx
index 1fa2ac205cc..5cf41de71b9 100644
--- a/packages/@react-spectrum/table/stories/TableDnDExamples.tsx
+++ b/packages/@react-spectrum/table/stories/TableDnDExamples.tsx
@@ -29,7 +29,7 @@ let columnsWithOutRowHeader = [
   {name: 'IP Address', key: 'ip_address'}
 ];
 
-let items = [
+export let items = [
   {id: 'a', first_name: 'Vin', last_name: 'Charlet', email: 'vcharlet0@123-reg.co.uk', ip_address: '18.45.175.130', department: 'Services', job_title: 'Analog Circuit Design manager'},
   {id: 'b', first_name: 'Lexy', last_name: 'Maddison', email: 'lmaddison1@xinhuanet.com', ip_address: '238.210.151.48', department: 'Research and Development', job_title: 'Analog Circuit Design manager'},
   {id: 'c', first_name: 'Robbi', last_name: 'Persence', email: 'rpersence2@hud.gov', ip_address: '130.2.120.99', department: 'Business Development', job_title: 'Analog Circuit Design manager'},
@@ -115,7 +115,7 @@ export function DragWithoutRowHeaderExample(props?)  {
 export function ReorderExample(props) {
   let {onDrop, onDragStart, onDragEnd, tableViewProps} = props;
   let list = useListData({
-    initialItems: items,
+    initialItems: (props.items as typeof items) || items,
     getKey: item => item.id
   });
 
diff --git a/packages/@react-stately/layout/src/GridLayout.ts b/packages/@react-stately/layout/src/GridLayout.ts
index bfbcceed306..3cf3607a99e 100644
--- a/packages/@react-stately/layout/src/GridLayout.ts
+++ b/packages/@react-stately/layout/src/GridLayout.ts
@@ -61,7 +61,7 @@ export class GridLayout<T, O = any> extends Layout<Node<T>, O> implements DropTa
     this.dropIndicatorThickness = options.dropIndicatorThickness || 2;
   }
 
-  validate(): void {
+  update(): void {
     let visibleWidth = this.virtualizer.visibleRect.width;
 
     // The max item width is always the entire viewport.
diff --git a/packages/@react-stately/layout/src/ListLayout.ts b/packages/@react-stately/layout/src/ListLayout.ts
index e3f452b0a91..dd105cf24e3 100644
--- a/packages/@react-stately/layout/src/ListLayout.ts
+++ b/packages/@react-stately/layout/src/ListLayout.ts
@@ -162,7 +162,7 @@ export class ListLayout<T, O = any> extends Layout<Node<T>, O> implements DropTa
     return invalidationContext.sizeChanged;
   }
 
-  validate(invalidationContext: InvalidationContext<O>) {
+  update(invalidationContext: InvalidationContext<O>) {
     this.collection = this.virtualizer.collection;
 
     // Reset valid rect if we will have to invalidate everything.
diff --git a/packages/@react-stately/layout/src/TableLayout.ts b/packages/@react-stately/layout/src/TableLayout.ts
index 8087889dad4..489b51cd16a 100644
--- a/packages/@react-stately/layout/src/TableLayout.ts
+++ b/packages/@react-stately/layout/src/TableLayout.ts
@@ -46,7 +46,7 @@ export class TableLayout<T, O extends TableLayoutProps = TableLayoutProps> exten
       );
   }
 
-  validate(invalidationContext: InvalidationContext<O>): void {
+  update(invalidationContext: InvalidationContext<O>): void {
     let newCollection = this.virtualizer.collection as TableCollection<T>;
 
     // If columnWidths were provided via layoutOptions, update those.
@@ -62,7 +62,7 @@ export class TableLayout<T, O extends TableLayoutProps = TableLayoutProps> exten
       invalidationContext.sizeChanged = true;
     }
 
-    super.validate(invalidationContext);
+    super.update(invalidationContext);
   }
 
   protected buildCollection(): LayoutNode[] {
@@ -227,7 +227,7 @@ export class TableLayout<T, O extends TableLayoutProps = TableLayoutProps> exten
     let width = 0;
     let children: LayoutNode[] = [];
     let rowHeight = this.getEstimatedRowHeight();
-    for (let [i, node] of [...getChildNodes(this.collection.body, this.collection)].entries()) {
+    for (let node of getChildNodes(this.collection.body, this.collection)) {
       // Skip rows before the valid rectangle unless they are already cached.
       if (y + rowHeight < this.requestedRect.y && !this.isValid(node, y)) {
         y += rowHeight;
@@ -237,7 +237,7 @@ export class TableLayout<T, O extends TableLayoutProps = TableLayoutProps> exten
 
       let layoutNode = this.buildChild(node, 0, y, layoutInfo.key);
       layoutNode.layoutInfo.parentKey = layoutInfo.key;
-      layoutNode.index = i;
+      layoutNode.index = children.length;
       y = layoutNode.layoutInfo.rect.maxY;
       width = Math.max(width, layoutNode.layoutInfo.rect.width);
       children.push(layoutNode);
@@ -285,7 +285,7 @@ export class TableLayout<T, O extends TableLayoutProps = TableLayoutProps> exten
 
     let children: LayoutNode[] = [];
     let height = 0;
-    for (let [i, child] of [...getChildNodes(node, this.collection)].entries()) {
+    for (let child of getChildNodes(node, this.collection)) {
       if (child.type === 'cell') {
         if (x > this.requestedRect.maxX) {
           // Adjust existing cached layoutInfo to ensure that it is out of view.
@@ -299,7 +299,7 @@ export class TableLayout<T, O extends TableLayoutProps = TableLayoutProps> exten
           let layoutNode = this.buildChild(child, x, y, layoutInfo.key);
           x = layoutNode.layoutInfo.rect.maxX;
           height = Math.max(height, layoutNode.layoutInfo.rect.height);
-          layoutNode.index = i;
+          layoutNode.index = children.length;
           children.push(layoutNode);
         }
       }
diff --git a/packages/@react-stately/virtualizer/src/Layout.ts b/packages/@react-stately/virtualizer/src/Layout.ts
index 806a9b0becb..1cb27f9b865 100644
--- a/packages/@react-stately/virtualizer/src/Layout.ts
+++ b/packages/@react-stately/virtualizer/src/Layout.ts
@@ -52,7 +52,7 @@ export abstract class Layout<T extends object, O = any> implements LayoutDelegat
    * Called by the virtualizer before {@link getVisibleLayoutInfos}
    * or {@link getLayoutInfo} are called.
    */
-  validate(invalidationContext: InvalidationContext<O>) {} // eslint-disable-line @typescript-eslint/no-unused-vars
+  update(invalidationContext: InvalidationContext<O>) {} // eslint-disable-line @typescript-eslint/no-unused-vars
 
   /**
    * Returns an array of {@link LayoutInfo} objects which are inside the given rectangle.
diff --git a/packages/@react-stately/virtualizer/src/Virtualizer.ts b/packages/@react-stately/virtualizer/src/Virtualizer.ts
index 4626c0e482a..c77aa305e5c 100644
--- a/packages/@react-stately/virtualizer/src/Virtualizer.ts
+++ b/packages/@react-stately/virtualizer/src/Virtualizer.ts
@@ -147,8 +147,8 @@ export class Virtualizer<T extends object, V> {
   }
 
   private relayout(context: InvalidationContext = {}) {
-    // Validate the layout
-    this.layout.validate(context);
+    // Update the layout
+    this.layout.update(context);
     (this as Mutable<this>).contentSize = this.layout.getContentSize();
 
     // Constrain scroll position.
diff --git a/packages/@react-stately/virtualizer/src/useVirtualizerState.ts b/packages/@react-stately/virtualizer/src/useVirtualizerState.ts
index 3a5485e362e..dff243c91a2 100644
--- a/packages/@react-stately/virtualizer/src/useVirtualizerState.ts
+++ b/packages/@react-stately/virtualizer/src/useVirtualizerState.ts
@@ -25,7 +25,7 @@ interface VirtualizerProps<T extends object, V, O> {
   layout: Layout<T>,
   collection: Collection<T>,
   onVisibleRectChange(rect: Rect): void,
-  persistedKeys?: Set<Key>,
+  persistedKeys?: Set<Key> | null,
   layoutOptions?: O
 }
 
diff --git a/packages/react-aria-components/src/Collection.tsx b/packages/react-aria-components/src/Collection.tsx
index 7e4837ea1ad..638ff819529 100644
--- a/packages/react-aria-components/src/Collection.tsx
+++ b/packages/react-aria-components/src/Collection.tsx
@@ -12,7 +12,7 @@
 import {CollectionBase, DropTargetDelegate, ItemDropTarget, Key, LayoutDelegate} from '@react-types/shared';
 import {createBranchComponent, useCachedChildren} from '@react-aria/collections';
 import {Collection as ICollection, Node, SelectionBehavior, SelectionMode, SectionProps as SharedSectionProps} from 'react-stately';
-import React, {createContext, ForwardedRef, HTMLAttributes, JSX, ReactElement, ReactNode, RefObject, useContext} from 'react';
+import React, {createContext, ForwardedRef, HTMLAttributes, JSX, ReactElement, ReactNode, RefObject, useContext, useMemo} from 'react';
 import {StyleProps} from './utils';
 
 export interface CollectionProps<T> extends Omit<CollectionBase<T>, 'children'> {
@@ -104,23 +104,35 @@ export const Section = /*#__PURE__*/ createBranchComponent('section', <T extends
 });
 
 export interface CollectionBranchProps {
+  /** The collection of items to render. */
   collection: ICollection<Node<unknown>>,
+  /** The parent node of the items to render. */
   parent: Node<unknown>,
+  /** A function that renders a drop indicator between items. */
   renderDropIndicator?: (target: ItemDropTarget) => ReactNode
 }
 
 export interface CollectionRootProps extends HTMLAttributes<HTMLElement> {
+  /** The collection of items to render. */
   collection: ICollection<Node<unknown>>,
-  focusedKey?: Key | null,
+  /** A set of keys for items that should always be persisted in the DOM. */
+  persistedKeys?: Set<Key> | null,
+  /** A ref to the scroll container for the collection. */
   scrollRef?: RefObject<HTMLElement | null>,
+  /** A function that renders a drop indicator between items. */
   renderDropIndicator?: (target: ItemDropTarget) => ReactNode
 }
 
 export interface CollectionRenderer {
+  /** Whether this is a virtualized collection. */
   isVirtualized?: boolean,
+  /** A delegate object that provides layout information for items in the collection. */
   layoutDelegate?: LayoutDelegate,
+  /** A delegate object that provides drop targets for pointer coordinates within the collection. */
   dropTargetDelegate?: DropTargetDelegate,
+  /** A component that renders the root collection items. */
   CollectionRoot: React.ComponentType<CollectionRootProps>,
+   /** A component that renders the child collection items. */
   CollectionBranch: React.ComponentType<CollectionBranchProps>
 }
 
@@ -160,3 +172,7 @@ function useCollectionRender(
 }
 
 export const CollectionRendererContext = createContext<CollectionRenderer>(DefaultCollectionRenderer);
+
+export function usePersistedKeys(focusedKey: Key) {
+  return useMemo(() => focusedKey != null ? new Set([focusedKey]) : null, [focusedKey]);
+}
diff --git a/packages/react-aria-components/src/DragAndDrop.tsx b/packages/react-aria-components/src/DragAndDrop.tsx
index d83303e9ea9..f11546ebde9 100644
--- a/packages/react-aria-components/src/DragAndDrop.tsx
+++ b/packages/react-aria-components/src/DragAndDrop.tsx
@@ -9,10 +9,10 @@
  * OF ANY KIND, either express or implied. See the License for the specific language
  * governing permissions and limitations under the License.
  */
-import type {DropIndicatorProps as AriaDropIndicatorProps, ItemDropTarget} from 'react-aria';
+import type {DropIndicatorProps as AriaDropIndicatorProps, ItemDropTarget, Key} from 'react-aria';
 import type {DragAndDropHooks} from './useDragAndDrop';
 import type {DraggableCollectionState, DroppableCollectionState, MultipleSelectionManager} from 'react-stately';
-import React, {createContext, ForwardedRef, forwardRef, JSX, ReactNode, useCallback, useContext} from 'react';
+import React, {createContext, ForwardedRef, forwardRef, JSX, ReactNode, useCallback, useContext, useMemo} from 'react';
 import type {RenderProps} from './utils';
 
 export interface DragAndDropContextValue {
@@ -62,9 +62,19 @@ export function useRenderDropIndicator(dragAndDropHooks?: DragAndDropHooks, drop
   return dragAndDropHooks?.useDropIndicator ? fn : undefined;
 }
 
-export function useDndAwareFocusedKey(selectionManager: MultipleSelectionManager, dragAndDropHooks?: DragAndDropHooks, dropState?: DroppableCollectionState) {
-  // Use drop target key during drag sessions so virtualizer persisted keys enable keyboard navigation to work correctly.
-  return dragAndDropHooks?.isVirtualDragging?.() && dropState?.target?.type === 'item'
-    ? dropState.target.key
-    : selectionManager.focusedKey;
+export function useDndPersistedKeys(selectionManager: MultipleSelectionManager, dragAndDropHooks?: DragAndDropHooks, dropState?: DroppableCollectionState) {
+  // Persist the focused key and the drop target key.
+  let focusedKey = selectionManager.focusedKey;
+  let dropTargetKey: Key | null = null;
+  if (dragAndDropHooks?.isVirtualDragging?.() && dropState?.target?.type === 'item') {
+    dropTargetKey = dropState.target.key;
+    if (dropState.target.dropPosition === 'after') {
+      // Normalize to the "before" drop position since we only render those to the DOM.
+      dropTargetKey = dropState.collection.getKeyAfter(dropTargetKey) ?? dropTargetKey;
+    }
+  }
+
+  return useMemo(() => {
+    return new Set([focusedKey, dropTargetKey].filter(k => k !== null));
+  }, [focusedKey, dropTargetKey]);
 }
diff --git a/packages/react-aria-components/src/GridList.tsx b/packages/react-aria-components/src/GridList.tsx
index 261c5aa49db..376a48b09e4 100644
--- a/packages/react-aria-components/src/GridList.tsx
+++ b/packages/react-aria-components/src/GridList.tsx
@@ -15,7 +15,7 @@ import {CheckboxContext} from './RSPContexts';
 import {Collection, CollectionBuilder, createLeafComponent} from '@react-aria/collections';
 import {CollectionProps, CollectionRendererContext, DefaultCollectionRenderer, ItemRenderProps} from './Collection';
 import {ContextValue, DEFAULT_SLOT, Provider, RenderProps, ScrollableProps, SlotProps, StyleRenderProps, useContextProps, useRenderProps} from './utils';
-import {DragAndDropContext, DropIndicatorContext, DropIndicatorProps, useDndAwareFocusedKey, useRenderDropIndicator} from './DragAndDrop';
+import {DragAndDropContext, DropIndicatorContext, DropIndicatorProps, useDndPersistedKeys, useRenderDropIndicator} from './DragAndDrop';
 import {DragAndDropHooks} from './useDragAndDrop';
 import {DraggableCollectionState, DroppableCollectionState, Collection as ICollection, ListState, Node, SelectionBehavior, useListState} from 'react-stately';
 import {filterDOMProps, useObjectRef} from '@react-aria/utils';
@@ -232,7 +232,7 @@ function GridListInner<T extends object>({props, collection, gridListRef: ref}:
           <CollectionRoot
             collection={collection}
             scrollRef={ref}
-            focusedKey={useDndAwareFocusedKey(selectionManager, dragAndDropHooks, dropState)}
+            persistedKeys={useDndPersistedKeys(selectionManager, dragAndDropHooks, dropState)}
             renderDropIndicator={useRenderDropIndicator(dragAndDropHooks, dropState)} />
         </Provider>
         {emptyState}
diff --git a/packages/react-aria-components/src/ListBox.tsx b/packages/react-aria-components/src/ListBox.tsx
index 16f19cb60a4..c48a2d15cfd 100644
--- a/packages/react-aria-components/src/ListBox.tsx
+++ b/packages/react-aria-components/src/ListBox.tsx
@@ -14,7 +14,7 @@ import {AriaListBoxOptions, AriaListBoxProps, DraggableItemResult, DragPreviewRe
 import {Collection, CollectionBuilder, createLeafComponent} from '@react-aria/collections';
 import {CollectionProps, CollectionRendererContext, ItemRenderProps, SectionContext, SectionProps} from './Collection';
 import {ContextValue, Provider, RenderProps, ScrollableProps, SlotProps, StyleRenderProps, useContextProps, useRenderProps, useSlot} from './utils';
-import {DragAndDropContext, DropIndicatorContext, DropIndicatorProps, useDndAwareFocusedKey, useRenderDropIndicator} from './DragAndDrop';
+import {DragAndDropContext, DropIndicatorContext, DropIndicatorProps, useDndPersistedKeys, useRenderDropIndicator} from './DragAndDrop';
 import {DragAndDropHooks} from './useDragAndDrop';
 import {DraggableCollectionState, DroppableCollectionState, ListState, Node, Orientation, SelectionBehavior, useListState} from 'react-stately';
 import {filterDOMProps, useObjectRef} from '@react-aria/utils';
@@ -250,7 +250,7 @@ function ListBoxInner<T extends object>({state, props, listBoxRef}: ListBoxInner
           <CollectionRoot
             collection={collection}
             scrollRef={listBoxRef}
-            focusedKey={useDndAwareFocusedKey(selectionManager, dragAndDropHooks, dropState)}
+            persistedKeys={useDndPersistedKeys(selectionManager, dragAndDropHooks, dropState)}
             renderDropIndicator={useRenderDropIndicator(dragAndDropHooks, dropState)} />
         </Provider>
         {emptyState}
diff --git a/packages/react-aria-components/src/Menu.tsx b/packages/react-aria-components/src/Menu.tsx
index 5d2b9d8ca22..88656a91ec3 100644
--- a/packages/react-aria-components/src/Menu.tsx
+++ b/packages/react-aria-components/src/Menu.tsx
@@ -14,7 +14,7 @@
 import {AriaMenuProps, FocusScope, mergeProps, useFocusRing, useMenu, useMenuItem, useMenuSection, useMenuTrigger} from 'react-aria';
 import {MenuTriggerProps as BaseMenuTriggerProps, Collection as ICollection, Node, TreeState, useMenuTriggerState, useTreeState} from 'react-stately';
 import {Collection, CollectionBuilder, createBranchComponent, createLeafComponent} from '@react-aria/collections';
-import {CollectionProps, CollectionRendererContext, ItemRenderProps, SectionContext, SectionProps} from './Collection';
+import {CollectionProps, CollectionRendererContext, ItemRenderProps, SectionContext, SectionProps, usePersistedKeys} from './Collection';
 import {ContextValue, Provider, RenderProps, ScrollableProps, SlotProps, StyleProps, useContextProps, useRenderProps, useSlot, useSlottedContext} from './utils';
 import {filterDOMProps, useObjectRef, useResizeObserver} from '@react-aria/utils';
 import {forwardRefType, HoverEvents, Key, LinkDOMProps} from '@react-types/shared';
@@ -222,7 +222,10 @@ function MenuInner<T extends object>({props, collection, menuRef: ref}: MenuInne
             [SubmenuTriggerContext, {parentMenuRef: ref}],
             [MenuItemContext, null]
           ]}>
-          <CollectionRoot collection={collection} focusedKey={state.selectionManager.focusedKey} scrollRef={ref} />
+          <CollectionRoot
+            collection={collection}
+            persistedKeys={usePersistedKeys(state.selectionManager.focusedKey)}
+            scrollRef={ref} />
         </Provider>
       </div>
       <div ref={setPopoverContainer} style={{width: '100vw', position: 'absolute', top: 0, ...leftOffset}} />
diff --git a/packages/react-aria-components/src/Table.tsx b/packages/react-aria-components/src/Table.tsx
index 73c75053cdb..b10662ea109 100644
--- a/packages/react-aria-components/src/Table.tsx
+++ b/packages/react-aria-components/src/Table.tsx
@@ -7,7 +7,7 @@ import {CollectionProps, CollectionRendererContext, DefaultCollectionRenderer, I
 import {ColumnSize, ColumnStaticSize, TableCollection as ITableCollection, TableProps as SharedTableProps} from '@react-types/table';
 import {ContextValue, DEFAULT_SLOT, DOMProps, Provider, RenderProps, ScrollableProps, SlotProps, StyleProps, StyleRenderProps, useContextProps, useRenderProps} from './utils';
 import {DisabledBehavior, DraggableCollectionState, DroppableCollectionState, MultipleSelectionState, Node, SelectionBehavior, SelectionMode, SortDirection, TableState, useMultipleSelectionState, useTableColumnResizeState, useTableState} from 'react-stately';
-import {DragAndDropContext, DropIndicatorContext, DropIndicatorProps, useDndAwareFocusedKey, useRenderDropIndicator} from './DragAndDrop';
+import {DragAndDropContext, DropIndicatorContext, DropIndicatorProps, useDndPersistedKeys, useRenderDropIndicator} from './DragAndDrop';
 import {DragAndDropHooks} from './useDragAndDrop';
 import {DraggableItemResult, DragPreviewRenderer, DropIndicatorAria, DroppableCollectionResult, FocusScope, ListKeyboardDelegate, mergeProps, useFocusRing, useHover, useLocale, useLocalizedStringFormatter, useTable, useTableCell, useTableColumnHeader, useTableColumnResize, useTableHeaderRow, useTableRow, useTableRowGroup, useTableSelectAllCheckbox, useTableSelectionCheckbox, useVisuallyHidden} from 'react-aria';
 import {filterDOMProps, isScrollable, mergeRefs, useLayoutEffect, useObjectRef, useResizeObserver} from '@react-aria/utils';
@@ -483,7 +483,7 @@ function TableInner({props, forwardedRef: ref, selectionState, collection}: Tabl
           <CollectionRoot
             collection={collection}
             scrollRef={tableContainerContext?.scrollRef ?? ref}
-            focusedKey={useDndAwareFocusedKey(selectionManager, dragAndDropHooks, dropState)} />
+            persistedKeys={useDndPersistedKeys(selectionManager, dragAndDropHooks, dropState)} />
         </ElementType>
       </FocusScope>
       {dragPreview}
diff --git a/packages/react-aria-components/src/Tabs.tsx b/packages/react-aria-components/src/Tabs.tsx
index 28083387547..cfa70926594 100644
--- a/packages/react-aria-components/src/Tabs.tsx
+++ b/packages/react-aria-components/src/Tabs.tsx
@@ -13,7 +13,7 @@
 import {AriaLabelingProps, forwardRefType, Key, LinkDOMProps} from '@react-types/shared';
 import {AriaTabListProps, AriaTabPanelProps, mergeProps, Orientation, useFocusRing, useHover, useTab, useTabList, useTabPanel} from 'react-aria';
 import {Collection, CollectionBuilder, createHideableComponent, createLeafComponent} from '@react-aria/collections';
-import {CollectionProps, CollectionRendererContext} from './Collection';
+import {CollectionProps, CollectionRendererContext, usePersistedKeys} from './Collection';
 import {ContextValue, Provider, RenderProps, SlotProps, StyleRenderProps, useContextProps, useRenderProps, useSlottedContext} from './utils';
 import {filterDOMProps, useObjectRef} from '@react-aria/utils';
 import {Collection as ICollection, Node, TabListState, useTabListState} from 'react-stately';
@@ -231,7 +231,7 @@ function TabListInner<T extends object>({props, forwardedRef: ref}: TabListInner
       ref={objectRef}
       {...renderProps}
       data-orientation={orientation || undefined}>
-      <CollectionRoot collection={state.collection} focusedKey={state.selectionManager.focusedKey} />
+      <CollectionRoot collection={state.collection} persistedKeys={usePersistedKeys(state.selectionManager.focusedKey)} />
     </div>
   );
 }
diff --git a/packages/react-aria-components/src/TagGroup.tsx b/packages/react-aria-components/src/TagGroup.tsx
index 9cad5d01edc..6cfaf56fe5e 100644
--- a/packages/react-aria-components/src/TagGroup.tsx
+++ b/packages/react-aria-components/src/TagGroup.tsx
@@ -13,7 +13,7 @@
 import {AriaTagGroupProps, useFocusRing, useHover, useTag, useTagGroup} from 'react-aria';
 import {ButtonContext} from './Button';
 import {Collection, CollectionBuilder, createLeafComponent} from '@react-aria/collections';
-import {CollectionProps, CollectionRendererContext, DefaultCollectionRenderer, ItemRenderProps} from './Collection';
+import {CollectionProps, CollectionRendererContext, DefaultCollectionRenderer, ItemRenderProps, usePersistedKeys} from './Collection';
 import {ContextValue, DOMProps, Provider, RenderProps, SlotProps, StyleRenderProps, useContextProps, useRenderProps, useSlot} from './utils';
 import {filterDOMProps, mergeProps, useObjectRef} from '@react-aria/utils';
 import {forwardRefType, HoverEvents, Key, LinkDOMProps} from '@react-types/shared';
@@ -157,6 +157,8 @@ function TagListInner<T extends object>({props, forwardedRef}: TagListInnerProps
     values: renderValues
   });
 
+  let persistedKeys = usePersistedKeys(state.selectionManager.focusedKey);
+
   return (
     <div
       {...mergeProps(gridProps, focusProps)}
@@ -167,7 +169,7 @@ function TagListInner<T extends object>({props, forwardedRef}: TagListInnerProps
       data-focus-visible={isFocusVisible || undefined}>
       {state.collection.size === 0 && props.renderEmptyState 
         ? props.renderEmptyState(renderValues) 
-        : <CollectionRoot collection={state.collection} focusedKey={state.selectionManager.focusedKey} />}
+        : <CollectionRoot collection={state.collection} persistedKeys={persistedKeys} />}
     </div>
   );
 }
diff --git a/packages/react-aria-components/src/Tree.tsx b/packages/react-aria-components/src/Tree.tsx
index c8ee3a1b0b0..4eccc34c930 100644
--- a/packages/react-aria-components/src/Tree.tsx
+++ b/packages/react-aria-components/src/Tree.tsx
@@ -14,7 +14,7 @@ import {AriaTreeGridListProps, useTreeGridList, useTreeGridListItem} from '@reac
 import {ButtonContext} from './Button';
 import {CheckboxContext} from './RSPContexts';
 import {Collection, CollectionBuilder, createBranchComponent, createLeafComponent, NodeValue, useCachedChildren} from '@react-aria/collections';
-import {CollectionProps, CollectionRendererContext, DefaultCollectionRenderer, ItemRenderProps} from './Collection';
+import {CollectionProps, CollectionRendererContext, DefaultCollectionRenderer, ItemRenderProps, usePersistedKeys} from './Collection';
 import {ContextValue, DEFAULT_SLOT, Provider, RenderProps, ScrollableProps, SlotProps, StyleRenderProps, useContextProps, useRenderProps} from './utils';
 import {DisabledBehavior, Expandable, forwardRefType, HoverEvents, Key, LinkDOMProps} from '@react-types/shared';
 import {filterDOMProps, useObjectRef} from '@react-aria/utils';
@@ -241,7 +241,10 @@ function TreeInner<T extends object>({props, collection, treeRef: ref}: TreeInne
           values={[
             [UNSTABLE_TreeStateContext, state]
           ]}>
-          <CollectionRoot collection={state.collection} focusedKey={state.selectionManager.focusedKey} scrollRef={ref} />
+          <CollectionRoot
+            collection={state.collection}
+            persistedKeys={usePersistedKeys(state.selectionManager.focusedKey)}
+            scrollRef={ref} />
         </Provider>
         {emptyState}
       </div>
diff --git a/packages/react-aria-components/src/Virtualizer.tsx b/packages/react-aria-components/src/Virtualizer.tsx
index 536b7eb6d3d..37f8a281752 100644
--- a/packages/react-aria-components/src/Virtualizer.tsx
+++ b/packages/react-aria-components/src/Virtualizer.tsx
@@ -25,7 +25,9 @@ export interface LayoutOptionsDelegate<O> {
 interface ILayout<O> extends Layout<Node<unknown>, O>, Partial<DropTargetDelegate>, LayoutOptionsDelegate<O> {}
 
 export interface VirtualizerProps {
+  /** The child collection to virtualize (e.g. ListBox, GridList, or Table). */
   children: ReactNode,
+  /** The layout object that determines the position and size of the visible elements. */
   layout: ILayout<any>
 }
 
@@ -37,7 +39,7 @@ export function Virtualizer(props: VirtualizerProps) {
     isVirtualized: true,
     layoutDelegate: layout,
     dropTargetDelegate: layout.getDropTargetFromPoint ? layout as DropTargetDelegate : undefined,
-    CollectionRoot({collection, focusedKey, scrollRef, renderDropIndicator}) {
+    CollectionRoot({collection, persistedKeys, scrollRef, renderDropIndicator}) {
       let layoutOptions = layout.useLayoutOptions?.();
       let state = useVirtualizerState({
         layout,
@@ -52,7 +54,7 @@ export function Virtualizer(props: VirtualizerProps) {
             element.scrollTop = rect.y;
           }
         },
-        persistedKeys: useMemo(() => focusedKey != null ? new Set([focusedKey]) : new Set(), [focusedKey]),
+        persistedKeys,
         layoutOptions
       });