diff --git a/drivers/overlay/composefs_notsupported.go b/drivers/overlay/composefs_notsupported.go
index 273ef4699d..75eae0affb 100644
--- a/drivers/overlay/composefs_notsupported.go
+++ b/drivers/overlay/composefs_notsupported.go
@@ -18,3 +18,7 @@ func generateComposeFsBlob(toc []byte, destFile string) error {
 func mountErofsBlob(blobFile, mountPoint string) error {
 	return fmt.Errorf("composefs is not supported")
 }
+
+func enableVerityRecursive(path string) error {
+	return fmt.Errorf("composefs is not supported")
+}
diff --git a/drivers/overlay/composefs_supported.go b/drivers/overlay/composefs_supported.go
index 7ecde856d1..c36c43b69b 100644
--- a/drivers/overlay/composefs_supported.go
+++ b/drivers/overlay/composefs_supported.go
@@ -5,12 +5,18 @@ package overlay
 
 import (
 	"bytes"
+	"errors"
 	"fmt"
+	"io/fs"
 	"os"
 	"os/exec"
+	"path/filepath"
 	"sync"
+	"syscall"
+	"unsafe"
 
 	"github.com/containers/storage/pkg/loopback"
+	"github.com/sirupsen/logrus"
 	"golang.org/x/sys/unix"
 )
 
@@ -32,6 +38,43 @@ func composeFsSupported() bool {
 	return err == nil
 }
 
+func enableVerity(description string, fd int) error {
+	enableArg := unix.FsverityEnableArg{
+		Version:        1,
+		Hash_algorithm: unix.FS_VERITY_HASH_ALG_SHA256,
+		Block_size:     4096,
+	}
+
+	_, _, e1 := syscall.Syscall(unix.SYS_IOCTL, uintptr(fd), uintptr(unix.FS_IOC_ENABLE_VERITY), uintptr(unsafe.Pointer(&enableArg)))
+	if e1 != 0 && !errors.Is(e1, unix.EEXIST) {
+		return fmt.Errorf("failed to enable verity for %q: %w", description, e1)
+	}
+	return nil
+}
+
+func enableVerityRecursive(path string) error {
+	walkFn := func(path string, d fs.DirEntry, err error) error {
+		if err != nil {
+			return err
+		}
+		if !d.Type().IsRegular() {
+			return nil
+		}
+
+		f, err := os.Open(path)
+		if err != nil {
+			return err
+		}
+		defer f.Close()
+
+		if err := enableVerity(path, int(f.Fd())); err != nil {
+			return err
+		}
+		return nil
+	}
+	return filepath.WalkDir(path, walkFn)
+}
+
 func generateComposeFsBlob(toc []byte, destFile string) error {
 	writerJson, err := getComposeFsHelper()
 	if err != nil {
@@ -44,14 +87,35 @@ func generateComposeFsBlob(toc []byte, destFile string) error {
 	}
 	outFd := os.NewFile(uintptr(fd), "outFd")
 
-	defer outFd.Close()
-	cmd := exec.Command(writerJson, "--format=erofs", "--out=/proc/self/fd/3", "/proc/self/fd/0")
-	cmd.ExtraFiles = []*os.File{outFd}
-	cmd.Stdin = bytes.NewReader(toc)
-	cmd.Stderr = os.Stderr
-	if err := cmd.Run(); err != nil {
-		return fmt.Errorf("failed to convert json to erofs: %w", err)
+	fd, err = unix.Open(fmt.Sprintf("/proc/self/fd/%d", outFd.Fd()), unix.O_RDONLY|unix.O_CLOEXEC, 0)
+	if err != nil {
+		outFd.Close()
+		return fmt.Errorf("failed to dup output file: %w", err)
+	}
+	newFd := os.NewFile(uintptr(fd), "newFd")
+	defer newFd.Close()
+
+	err = func() error {
+		// a scope to close outFd before setting fsverity on the read-only fd.
+		defer outFd.Close()
+
+		cmd := exec.Command(writerJson, "--format=erofs", "--out=/proc/self/fd/3", "/proc/self/fd/0")
+		cmd.ExtraFiles = []*os.File{outFd}
+		cmd.Stderr = os.Stderr
+		cmd.Stdin = bytes.NewReader(toc)
+		if err := cmd.Run(); err != nil {
+			return fmt.Errorf("failed to convert json to erofs: %w", err)
+		}
+		return nil
+	}()
+	if err != nil {
+		return err
 	}
+
+	if err := enableVerity("manifest file", int(newFd.Fd())); err != nil && !errors.Is(err, unix.ENOTSUP) && !errors.Is(err, unix.ENOTTY) {
+		logrus.Warningf("%s", err)
+	}
+
 	return nil
 }
 
diff --git a/drivers/overlay/overlay.go b/drivers/overlay/overlay.go
index a4e6b7d3ca..3170f09645 100644
--- a/drivers/overlay/overlay.go
+++ b/drivers/overlay/overlay.go
@@ -2064,6 +2064,11 @@ func (d *Driver) ApplyDiffFromStagingDirectory(id, parent, stagingDirectory stri
 	}
 
 	if d.useComposeFs() {
+		// FIXME: move this logic into the differ so we don't have to open
+		// the file twice.
+		if err := enableVerityRecursive(stagingDirectory); err != nil && !errors.Is(err, unix.ENOTSUP) && !errors.Is(err, unix.ENOTTY) {
+			logrus.Warningf("%s", err)
+		}
 		toc := diffOutput.BigData[zstdChunkedManifest]
 		if err := generateComposeFsBlob(toc, d.getErofsBlob(id)); err != nil {
 			return err