diff --git a/orbit/cmd/orbit/orbit.go b/orbit/cmd/orbit/orbit.go
index 2f8a7ad37b8e..21cfa8858033 100644
--- a/orbit/cmd/orbit/orbit.go
+++ b/orbit/cmd/orbit/orbit.go
@@ -471,13 +471,26 @@ func main() {
 			}
 		}
 
-		metadataFileName := update.MetadataFileName
 		if updateURL := c.String("update-url"); updateURL != update.OldFleetTUFURL && updateURL != update.DefaultURL {
-			// Users using custom TUF repository will continue using the local TUF metadata as usual.
-			metadataFileName = update.OldMetadataFileName
+			// Migrate agents running with a custom TUF to use the new metadata file.
+			// We'll keep the old metadata file to support downgrades.
+			newMetadataFilePath := filepath.Join(c.String("root-dir"), update.MetadataFileName)
+			ok, err := file.Exists(newMetadataFilePath)
+			if err != nil {
+				// If we cannot stat this file then we cannot do other operations on it thus we fail with fatal error.
+				log.Fatal().Err(err).Msg("failed to check for new metadata file path")
+			}
+			if !ok {
+				oldMetadataFilePath := filepath.Join(c.String("root-dir"), update.OldMetadataFileName)
+				err := file.Copy(oldMetadataFilePath, newMetadataFilePath, constant.DefaultFileMode)
+				if err != nil {
+					// If we cannot write to this file then we cannot do other operations on it thus we fail with fatal error.
+					log.Fatal().Err(err).Msg("failed to copy new metadata file path")
+				}
+			}
 		}
 
-		localStore, err := filestore.New(filepath.Join(c.String("root-dir"), metadataFileName))
+		localStore, err := filestore.New(filepath.Join(c.String("root-dir"), update.MetadataFileName))
 		if err != nil {
 			log.Fatal().Err(err).Msg("create local metadata store")
 		}
@@ -510,7 +523,7 @@ func main() {
 		opt.RootDirectory = c.String("root-dir")
 		opt.ServerURL = c.String("update-url")
 		if opt.ServerURL == update.OldFleetTUFURL {
-			// orbit 1.37.0+ will use the new TUF repository
+			// orbit 1.38.0+ will use the new TUF repository
 			opt.ServerURL = update.DefaultURL
 		}
 		opt.LocalStore = localStore
diff --git a/orbit/pkg/packaging/packaging.go b/orbit/pkg/packaging/packaging.go
index 110518f51609..279da1dc5e71 100644
--- a/orbit/pkg/packaging/packaging.go
+++ b/orbit/pkg/packaging/packaging.go
@@ -172,12 +172,7 @@ func (u UpdatesData) String() string {
 }
 
 func InitializeUpdates(updateOpt update.Options) (*UpdatesData, error) {
-	metadataFileName := update.MetadataFileName
-	if updateOpt.ServerURL != update.OldFleetTUFURL && updateOpt.ServerURL != update.DefaultURL {
-		// Users using custom TUF repository will continue using the local TUF metadata as usual.
-		metadataFileName = update.OldMetadataFileName
-	}
-	localStore, err := filestore.New(filepath.Join(updateOpt.RootDirectory, metadataFileName))
+	localStore, err := filestore.New(filepath.Join(updateOpt.RootDirectory, update.MetadataFileName))
 	if err != nil {
 		return nil, fmt.Errorf("failed to create local metadata store: %w", err)
 	}
@@ -241,14 +236,15 @@ func InitializeUpdates(updateOpt update.Options) (*UpdatesData, error) {
 		}
 	}
 
-	if updateOpt.ServerURL == update.OldFleetTUFURL || updateOpt.ServerURL == update.DefaultURL {
-		// If using Fleet's TUF then copy the new metadata to the old location (pre-migration) to
-		// support orbit downgrades to 1.36.0 or lower.
-		oldMetadataPath := filepath.Join(updateOpt.RootDirectory, update.OldMetadataFileName)
-		newMetadataPath := filepath.Join(updateOpt.RootDirectory, update.MetadataFileName)
-		if err := file.Copy(newMetadataPath, oldMetadataPath, constant.DefaultFileMode); err != nil {
-			return nil, fmt.Errorf("failed to create %s copy: %w", oldMetadataPath, err)
-		}
+	// Copy the new metadata file to the old location (pre-migration) to
+	// support orbit downgrades to 1.37.0 or lower.
+	//
+	// Once https://tuf.fleetctl.com is brought down (which means downgrades to 1.37.0 or
+	// lower won't be possible), we can remove this copy.
+	oldMetadataPath := filepath.Join(updateOpt.RootDirectory, update.OldMetadataFileName)
+	newMetadataPath := filepath.Join(updateOpt.RootDirectory, update.MetadataFileName)
+	if err := file.Copy(newMetadataPath, oldMetadataPath, constant.DefaultFileMode); err != nil {
+		return nil, fmt.Errorf("failed to create %s copy: %w", oldMetadataPath, err)
 	}
 
 	return &UpdatesData{
diff --git a/orbit/pkg/update/update.go b/orbit/pkg/update/update.go
index 50de47008aff..a45e5c117a43 100644
--- a/orbit/pkg/update/update.go
+++ b/orbit/pkg/update/update.go
@@ -39,8 +39,22 @@ const (
 // Defining these as variables so that we can overwrite them during development/testing of the migration.
 var (
 	//
-	// These used by `fleetctl package` and by orbit in the migration to the new TUF repository.
+	// For users using Fleet's TUF:
+	// 	- orbit 1.38.0+ we migrate TUF from https://tuf.fleetctl.com to https://updates.fleetdm.com.
+	//	- orbit 1.38.0+ will start using `updates-metadata.json` instead of `tuf-metadata.json`. If it is missing
+	//	(which will be the case for the first run after the auto-update) then it will generate it from the new pinned roots.
 	//
+	// For users using a custom TUF:
+	//	- orbit 1.38.0+ will start using `updates-metadata.json` instead of `tuf-metadata.json` (if it is missing then
+	// 	  it will perform a copy).
+	//
+	// For both Fleet's TUF and custom TUF, fleetd packages built with fleetctl 4.62.0+ will contain both files
+	// `updates-metadata.json` and `tuf-metadata.json` (same content) to support downgrades to orbit 1.37.0 or lower.
+
+	//
+	// The following variables are used by `fleetctl package` and by orbit in the migration to the new TUF repository.
+	//
+
 	// TODO(lucas): Before merging to `main` update DefaultURL to "https://updates.fleetctl.com".
 	DefaultURL       = `https://tuf.fleetctl.com`
 	MetadataFileName = "updates-metadata.json"
diff --git a/tools/tuf/test/migration/migration_test.sh b/tools/tuf/test/migration/migration_test.sh
index 146b5b63be13..ae44d726d2e0 100755
--- a/tools/tuf/test/migration/migration_test.sh
+++ b/tools/tuf/test/migration/migration_test.sh
@@ -5,6 +5,7 @@
 #   - User runs the script on macOS
 #   - User has a Ubuntu 22.04 and a Windows 10/11 VM (running on the same macOS host script runs on).
 #   - Fleet is running on the macOS host.
+#   - `fleetctl login` was ran on the localhost Fleet instance (to be able to run `fleectl query` commands).
 #   - host.docker.internal points to localhost on the macOS host.
 #   - host.docker.internal points to the macOS host on the two VMs (/etc/hosts on Ubuntu and C:\Windows\System32\Drivers\etc\hosts on Windows).
 #   - 1.36.0 is the last version of orbit that uses the old TUF repository