diff --git a/editor/filesystem_dock.cpp b/editor/filesystem_dock.cpp
index 8d4a2a9c500..6b6abd47620 100644
--- a/editor/filesystem_dock.cpp
+++ b/editor/filesystem_dock.cpp
@@ -3242,6 +3242,10 @@ void FileSystemDock::_file_and_folders_fill_popup(PopupMenu *p_popup, const Vect
 		p_popup->add_separator();
 	}
 
+	// Check if the root path is selected, we must check p_paths[1] because the first string in
+	// the list of paths obtained by _tree_get_selected(...) is not always the root path.
+	bool root_path_not_selected = p_paths[0] != "res://" && (p_paths.size() <= 1 || p_paths[1] != "res://");
+
 	if (all_folders && foldernames.size() > 0) {
 		p_popup->add_icon_item(get_editor_theme_icon(SNAME("Load")), TTR("Expand Folder"), FILE_OPEN);
 
@@ -3252,7 +3256,8 @@ void FileSystemDock::_file_and_folders_fill_popup(PopupMenu *p_popup, const Vect
 
 		p_popup->add_separator();
 
-		if (p_paths[0] != "res://") {
+		// Only add the 'Set Folder Color...' option if the root path is not selected.
+		if (root_path_not_selected) {
 			PopupMenu *folder_colors_menu = memnew(PopupMenu);
 			folder_colors_menu->connect(SceneStringName(id_pressed), callable_mp(this, &FileSystemDock::_folder_color_index_pressed).bind(folder_colors_menu));
 
@@ -3272,25 +3277,31 @@ void FileSystemDock::_file_and_folders_fill_popup(PopupMenu *p_popup, const Vect
 		}
 	}
 
+	// Add the options that are only available when a single item is selected.
 	if (p_paths.size() == 1) {
 		p_popup->add_icon_shortcut(get_editor_theme_icon(SNAME("ActionCopy")), ED_GET_SHORTCUT("filesystem_dock/copy_path"), FILE_COPY_PATH);
 		p_popup->add_shortcut(ED_GET_SHORTCUT("filesystem_dock/copy_absolute_path"), FILE_COPY_ABSOLUTE_PATH);
 		if (ResourceLoader::get_resource_uid(p_paths[0]) != ResourceUID::INVALID_ID) {
 			p_popup->add_icon_shortcut(get_editor_theme_icon(SNAME("Instance")), ED_GET_SHORTCUT("filesystem_dock/copy_uid"), FILE_COPY_UID);
 		}
-		if (p_paths[0] != "res://") {
+		if (root_path_not_selected) {
 			p_popup->add_icon_shortcut(get_editor_theme_icon(SNAME("Rename")), ED_GET_SHORTCUT("filesystem_dock/rename"), FILE_RENAME);
 			p_popup->add_icon_shortcut(get_editor_theme_icon(SNAME("Duplicate")), ED_GET_SHORTCUT("filesystem_dock/duplicate"), FILE_DUPLICATE);
 		}
 	}
 
-	if (p_paths.size() > 1 || p_paths[0] != "res://") {
+	// Add the options that are only available when the root path is not selected.
+	if (root_path_not_selected) {
 		p_popup->add_icon_item(get_editor_theme_icon(SNAME("MoveUp")), TTR("Move/Duplicate To..."), FILE_MOVE);
 		p_popup->add_icon_shortcut(get_editor_theme_icon(SNAME("Remove")), ED_GET_SHORTCUT("filesystem_dock/delete"), FILE_REMOVE);
 	}
 
-	p_popup->add_separator();
+	// Only add a separator if we have actually placed any options in the menu since the last separator.
+	if (p_paths.size() == 1 || root_path_not_selected) {
+		p_popup->add_separator();
+	}
 
+	// Add the options that are available when one or more items are selected.
 	if (p_paths.size() >= 1) {
 		if (!all_favorites) {
 			p_popup->add_icon_item(get_editor_theme_icon(SNAME("Favorites")), TTR("Add to Favorites"), FILE_ADD_FAVORITE);
@@ -3299,7 +3310,7 @@ void FileSystemDock::_file_and_folders_fill_popup(PopupMenu *p_popup, const Vect
 			p_popup->add_icon_item(get_editor_theme_icon(SNAME("NonFavorite")), TTR("Remove from Favorites"), FILE_REMOVE_FAVORITE);
 		}
 
-		if (p_paths.size() > 1 || p_paths[0] != "res://") {
+		if (root_path_not_selected) {
 			cached_valid_conversion_targets = _get_valid_conversions_for_file_paths(p_paths);
 
 			int relative_id = 0;