diff --git a/docs/guide/api-environment-plugins.md b/docs/guide/api-environment-plugins.md
index 7a888cc213a03b..8ebe062667b072 100644
--- a/docs/guide/api-environment-plugins.md
+++ b/docs/guide/api-environment-plugins.md
@@ -146,7 +146,7 @@ The hook can choose to:
 
 ## Per-environment State in Plugins
 
-Given that the same plugin instance is used for different environments, the plugin state needs to be keyed with `this.environment`. This is the same pattern the ecosystem has already been using to keep state about modules using the `ssr` boolean as key to avoid mixing client and ssr modules state. A `Map<Environment, State>` can be used to keep the state for each environment separately. Note that for backward compatibility, `buildStart` and `buildEnd` are only called for the client environment without the `perEnvironmentStartEndDuringDev: true` flag.
+Given that the same plugin instance is used for different environments, the plugin state needs to be keyed with `this.environment`. This is the same pattern the ecosystem has already been using to keep state about modules using the `ssr` boolean as key to avoid mixing client and ssr modules state. A `Map<Environment, State>` can be used to keep the state for each environment separately. Note that for backward compatibility, `buildStart` and `buildEnd` are only called for the client environment without the `perEnvironmentStartEndDuringDev: true` flag. Same for `watchChange` and the `perEnvironmentWatchChangeDuringDev: true` flag.
 
 ```js
 function PerEnvironmentCountTransformedModulesPlugin() {
diff --git a/packages/vite/src/node/plugin.ts b/packages/vite/src/node/plugin.ts
index 08940187b54456..3ba44e3968da2b 100644
--- a/packages/vite/src/node/plugin.ts
+++ b/packages/vite/src/node/plugin.ts
@@ -176,6 +176,14 @@ export interface Plugin<A = any> extends RollupPlugin<A> {
    * @experimental
    */
   perEnvironmentStartEndDuringDev?: boolean
+  /**
+   * Opt-in this plugin into per-environment watchChange during dev.
+   * For backward-compatibility, the watchChange hook is called only once during
+   * dev, for the client environment. Plugins can opt-in to be called
+   * per-environment, aligning with the watchChange hook behavior.
+   * @experimental
+   */
+  perEnvironmentWatchChangeDuringDev?: boolean
   /**
    * Enforce plugin invocation tier similar to webpack loaders. Hooks ordering
    * is still subject to the `order` property in the hook object.
diff --git a/packages/vite/src/node/server/index.ts b/packages/vite/src/node/server/index.ts
index d0c2d0b29aaa67..27d694dea04541 100644
--- a/packages/vite/src/node/server/index.ts
+++ b/packages/vite/src/node/server/index.ts
@@ -174,12 +174,19 @@ export interface ServerOptions extends CommonServerOptions {
     | false
     | ((sourcePath: string, sourcemapPath: string) => boolean)
   /**
-   * Backward compatibility. The buildStart and buildEnd hooks were called only once for all
-   * environments. This option enables per-environment buildStart and buildEnd hooks.
+   * Backward compatibility. The buildStart and buildEnd hooks were called only once for
+   * the client environment. This option enables per-environment buildStart and buildEnd hooks.
    * @default false
    * @experimental
    */
   perEnvironmentStartEndDuringDev?: boolean
+  /**
+   * Backward compatibility. The watchChange hook was called only once for the client environment.
+   * This option enables per-environment watchChange hooks.
+   * @default false
+   * @experimental
+   */
+  perEnvironmentWatchChangeDuringDev?: boolean
   /**
    * Run HMR tasks, by default the HMR propagation is done in parallel for all environments
    * @experimental
@@ -802,9 +809,13 @@ export async function _createServer(
     file = normalizePath(file)
     reloadOnTsconfigChange(server, file)
 
-    await pluginContainer.watchChange(file, {
-      event: isUnlink ? 'delete' : 'create',
-    })
+    await Promise.all(
+      Object.values(server.environments).map((environment) =>
+        environment.pluginContainer.watchChange(file, {
+          event: isUnlink ? 'delete' : 'create',
+        }),
+      ),
+    )
 
     if (publicDir && publicFiles) {
       if (file.startsWith(publicDir)) {
@@ -836,7 +847,11 @@ export async function _createServer(
     file = normalizePath(file)
     reloadOnTsconfigChange(server, file)
 
-    await pluginContainer.watchChange(file, { event: 'update' })
+    await Promise.all(
+      Object.values(server.environments).map((environment) =>
+        environment.pluginContainer.watchChange(file, { event: 'update' }),
+      ),
+    )
     // invalidate module graph cache on file change
     for (const environment of Object.values(server.environments)) {
       environment.moduleGraph.onFileChange(file)
@@ -1104,6 +1119,7 @@ const _serverConfigDefaults = Object.freeze({
   preTransformRequests: true,
   // sourcemapIgnoreList
   perEnvironmentStartEndDuringDev: false,
+  perEnvironmentWatchChangeDuringDev: false,
   // hotUpdateEnvironments
 } satisfies ServerOptions)
 export const serverConfigDefaults: Readonly<Partial<ServerOptions>> =
diff --git a/packages/vite/src/node/server/pluginContainer.ts b/packages/vite/src/node/server/pluginContainer.ts
index a2d96cfdf9d6c8..05f24cc4c71bc5 100644
--- a/packages/vite/src/node/server/pluginContainer.ts
+++ b/packages/vite/src/node/server/pluginContainer.ts
@@ -607,10 +607,15 @@ class EnvironmentPluginContainer<Env extends Environment = Environment> {
     id: string,
     change: { event: 'create' | 'update' | 'delete' },
   ): Promise<void> {
+    const config = this.environment.getTopLevelConfig()
     await this.hookParallel(
       'watchChange',
       (plugin) => this._getPluginContext(plugin),
       () => [id, change],
+      (plugin) =>
+        this.environment.name === 'client' ||
+        config.server.perEnvironmentWatchChangeDuringDev ||
+        plugin.perEnvironmentWatchChangeDuringDev,
     )
   }
 
@@ -1211,7 +1216,8 @@ class PluginContainer {
   }
 
   // For backward compatibility, buildStart and watchChange are called only for the client environment
-  // buildStart is called per environment for a plugin with the perEnvironmentStartEndDuring dev flag
+  // buildStart is called per environment for a plugin with the perEnvironmentStartEndDuringDev flag
+  // watchChange is called per environment for a plugin with the perEnvironmentWatchChangeDuringDev flag
 
   async buildStart(_options?: InputOptions): Promise<void> {
     return (