diff --git a/metadata/updater/updater.go b/metadata/updater/updater.go
index bd533b63..bed0168b 100644
--- a/metadata/updater/updater.go
+++ b/metadata/updater/updater.go
@@ -148,7 +148,12 @@ func (update *Updater) onlineRefresh() error {
 // The metadata on disk are verified against the provided root though,
 // and expiration dates are verified.
 func (update *Updater) unsafeLocalRefresh() error {
-	// Root is already loaded
+	// Load any rotated roots from disk
+	err := update.loadRootFromDisk()
+	if err != nil {
+		return err
+	}
+
 	// load timestamp
 	var p = filepath.Join(update.cfg.LocalMetadataDir, metadata.TIMESTAMP)
 	data, err := update.loadLocalMetadata(p)
@@ -511,6 +516,45 @@ func (update *Updater) loadRoot() error {
 			if err != nil {
 				return err
 			}
+			// also persist versioned root for offline use (e.g., unsafe local mode)
+			versionedRootName := fmt.Sprintf("%d.%s", nextVersion, metadata.ROOT)
+			err = update.persistMetadata(versionedRootName, data)
+			if err != nil {
+				return err
+			}
+		}
+	}
+	return nil
+}
+
+// loadRootFromDisk loads root metadata from local disk. Sequentially loads and
+// verifies every newer root metadata version available on disk.
+// This is used by unsafe local mode to support root rotation when operating offline.
+func (update *Updater) loadRootFromDisk() error {
+	// calculate boundaries
+	lowerBound := update.trusted.Root.Signed.Version + 1
+	upperBound := lowerBound + update.cfg.MaxRootRotations
+
+	// loop until we find the latest available version of root on disk
+	for nextVersion := lowerBound; nextVersion < upperBound; nextVersion++ {
+		versionedRootName := fmt.Sprintf("%d.%s", nextVersion, metadata.ROOT)
+		rootPath := filepath.Join(update.cfg.LocalMetadataDir, fmt.Sprintf("%s.json", url.PathEscape(versionedRootName)))
+
+		// try to load versioned root from disk
+		data, err := os.ReadFile(rootPath)
+		if err != nil {
+			if os.IsNotExist(err) {
+				// no more root versions available on disk, stop the loop
+				break
+			}
+			// some other error occurred
+			return err
+		}
+
+		// verify and load the root metadata
+		_, err = update.trusted.UpdateRoot(data)
+		if err != nil {
+			return err
 		}
 	}
 	return nil
diff --git a/metadata/updater/updater_top_level_update_test.go b/metadata/updater/updater_top_level_update_test.go
index 214105b4..8c05eecd 100644
--- a/metadata/updater/updater_top_level_update_test.go
+++ b/metadata/updater/updater_top_level_update_test.go
@@ -293,8 +293,8 @@ func TestUnsafeRefresh(t *testing.T) {
 	for _, role := range metadata.TOP_LEVEL_ROLE_NAMES {
 		var version int
 		if role == metadata.ROOT {
-			// The root file is written when the updater is
-			// created, so the version is reset.
+			// The root file on disk is version 1 (written when updater was created).
+			// Unsafe mode doesn't persist to disk, it only loads from disk.
 			version = 1
 		}
 		assertContentEquals(t, role, &version)
@@ -303,12 +303,58 @@ func TestUnsafeRefresh(t *testing.T) {
 	assert.Equal(t, metadata.ROOT, updater.trusted.Root.Signed.Type)
 	assert.Equal(t, metadata.SPECIFICATION_VERSION, updater.trusted.Root.Signed.SpecVersion)
 	assert.True(t, updater.trusted.Root.Signed.ConsistentSnapshot)
-	assert.Equal(t, int64(1), updater.trusted.Root.Signed.Version)
+	// However, the in-memory trusted root should be version 2 after loading from disk
+	assert.Equal(t, int64(2), updater.trusted.Root.Signed.Version)
 	assert.NotNil(t, updater.trusted.Snapshot)
 	assert.NotNil(t, updater.trusted.Timestamp)
 	assert.Equal(t, 1, len(updater.trusted.Targets))
 }
 
+func TestUnsafeRefreshWithRotatedRoots(t *testing.T) {
+	// First run a "real" refresh to establish initial metadata
+	err := loadOrResetTrustedRootMetadata()
+	assert.NoError(t, err)
+
+	updaterConfig, err := loadUpdaterConfig()
+	assert.NoError(t, err)
+	_, err = runRefresh(updaterConfig, time.Now())
+	assert.NoError(t, err)
+	assertFilesExist(t, metadata.TOP_LEVEL_ROLE_NAMES[:])
+
+	// Bump root version without changing keys (simpler test case)
+	// This tests if unsafe mode can handle multiple root versions on disk
+	simulator.Sim.MDRoot.Signed.Version = 2
+	simulator.Sim.PublishRoot()
+
+	simulator.Sim.MDRoot.Signed.Version = 3
+	simulator.Sim.PublishRoot()
+
+	// Run another refresh in online mode to download the new root versions
+	// This ensures root.2.json and root.3.json are in the local cache
+	updaterConfig, err = loadUpdaterConfig()
+	assert.NoError(t, err)
+	onlineUpdater, err := runRefresh(updaterConfig, time.Now())
+	assert.NoError(t, err)
+	assert.Equal(t, int64(3), onlineUpdater.trusted.Root.Signed.Version)
+
+	// Now create a new unsafe updater with the original trusted root (version 1)
+	// and verify it loads the rotated roots from disk
+	updaterConfig, err = loadUnsafeUpdaterConfig()
+	assert.NoError(t, err)
+	unsafeUpdater, err := runRefresh(updaterConfig, time.Now())
+	assert.NoError(t, err)
+
+	// The key assertion: unsafe mode should load rotated roots from disk
+	// and end up with the latest root version
+	assert.Equal(t, int64(3), unsafeUpdater.trusted.Root.Signed.Version,
+		"Unsafe local mode should load rotated roots from disk")
+
+	// Verify the other metadata is properly loaded
+	assert.NotNil(t, unsafeUpdater.trusted.Timestamp)
+	assert.NotNil(t, unsafeUpdater.trusted.Snapshot)
+	assert.Equal(t, 1, len(unsafeUpdater.trusted.Targets))
+}
+
 func TestTrustedRootMissing(t *testing.T) {
 	err := loadOrResetTrustedRootMetadata()
 	assert.NoError(t, err)