diff --git a/wp-admin/site-editor.php b/wp-admin/site-editor.php
index d27f461c9f..5fc06a4078 100644
--- a/wp-admin/site-editor.php
+++ b/wp-admin/site-editor.php
@@ -182,7 +182,6 @@ $preload_paths = array(
 	array( rest_get_route_for_post_type_items( 'attachment' ), 'OPTIONS' ),
 	array( rest_get_route_for_post_type_items( 'page' ), 'OPTIONS' ),
 	'/wp/v2/types?context=view',
-	'/wp/v2/wp_registered_template?context=edit',
 	'/wp/v2/types/wp_template?context=edit',
 	'/wp/v2/types/wp_template_part?context=edit',
 	'/wp/v2/templates?context=edit&per_page=-1',
diff --git a/wp-includes/block-template-utils.php b/wp-includes/block-template-utils.php
index b0ca8c6caf..53954b7ff4 100644
--- a/wp-includes/block-template-utils.php
+++ b/wp-includes/block-template-utils.php
@@ -1358,8 +1358,6 @@ function get_block_template( $id, $template_type = 'wp_template' ) {
 					return $template;
 				}
 			}
-		} elseif ( false === $active_templates[ $slug ] ) {
-			return null;
 		}
 	}
 
@@ -1882,3 +1880,57 @@ function wp_maybe_activate_template( $post_id ) {
 	$active_templates[ $post->post_name ] = $post->ID;
 	update_option( 'active_templates', $active_templates );
 }
+
+function _wp_migrate_active_templates() {
+	// Do not run during installation when the database is not yet available.
+	if ( wp_installing() ) {
+		return;
+	}
+
+	$active_templates = get_option( 'active_templates', false );
+
+	if ( false !== $active_templates ) {
+		return;
+	}
+
+	// Query all templates in the database. See `get_block_templates`.
+	$wp_query_args = array(
+		'post_status'         => 'publish',
+		'post_type'           => 'wp_template',
+		'posts_per_page'      => -1,
+		'no_found_rows'       => true,
+		'lazy_load_term_meta' => false,
+		'tax_query'           => array(
+			array(
+				'taxonomy' => 'wp_theme',
+				'field'    => 'name',
+				'terms'    => get_stylesheet(),
+			),
+		),
+		// Only get templates that are not inactive by default. We check these
+		// meta to make sure we don't fill the option with inactive templates
+		// created after the 6.9 release when for some reason the option is
+		// deleted.
+		'meta_query'          => array(
+			'relation' => 'OR',
+			array(
+				'key'     => 'is_inactive_by_default',
+				'compare' => 'NOT EXISTS',
+			),
+			array(
+				'key'     => 'is_inactive_by_default',
+				'value'   => false,
+				'compare' => '=',
+			),
+		),
+	);
+
+	$template_query   = new WP_Query( $wp_query_args );
+	$active_templates = array();
+
+	foreach ( $template_query->posts as $post ) {
+		$active_templates[ $post->post_name ] = $post->ID;
+	}
+
+	update_option( 'active_templates', $active_templates );
+}
diff --git a/wp-includes/block-template.php b/wp-includes/block-template.php
index 2dd7b2e3c0..220cb0b2a2 100644
--- a/wp-includes/block-template.php
+++ b/wp-includes/block-template.php
@@ -164,20 +164,10 @@ function resolve_block_template( $template_type, $template_hierarchy, $fallback_
 		$template_hierarchy
 	);
 
-	$object            = get_queried_object();
-	$specific_template = $object ? get_page_template_slug( $object ) : null;
+	$object_id         = get_queried_object_id();
+	$specific_template = $object_id && get_post( $object_id ) ? get_page_template_slug( $object_id ) : null;
 	$active_templates  = (array) get_option( 'active_templates', array() );
 
-	// Remove templates slugs that are deactivated, except if it's the specific
-	// template or index.
-	$slugs = array_filter(
-		$slugs,
-		function ( $slug ) use ( $specific_template, $active_templates ) {
-			$should_ignore = $slug === $specific_template || 'index' === $slug;
-			return $should_ignore || ( ! isset( $active_templates[ $slug ] ) || false !== $active_templates[ $slug ] );
-		}
-	);
-
 	// We expect one template for each slug. Use the active template if it is
 	// set and exists. Otherwise use the static template.
 	$templates       = array();
@@ -232,7 +222,7 @@ function resolve_block_template( $template_type, $template_hierarchy, $fallback_
 	);
 	$templates = array_merge( $templates, get_registered_block_templates( $query ) );
 
-	if ( $specific_template ) {
+	if ( $specific_template && in_array( $specific_template, $remaining_slugs, true ) ) {
 		$templates = array_merge( $templates, get_block_templates( array( 'slug__in' => array( $specific_template ) ) ) );
 	}
 
diff --git a/wp-includes/default-filters.php b/wp-includes/default-filters.php
index 4a386eb53c..5dc54c3686 100644
--- a/wp-includes/default-filters.php
+++ b/wp-includes/default-filters.php
@@ -570,6 +570,7 @@ add_action( 'transition_post_status', '__clear_multi_author_cache' );
 
 // Post.
 add_action( 'init', 'create_initial_post_types', 0 ); // Highest priority.
+add_action( 'init', '_wp_migrate_active_templates', 0 ); // Highest priority.
 add_action( 'admin_menu', '_add_post_type_submenus' );
 add_action( 'before_delete_post', '_reset_front_page_settings_for_post' );
 add_action( 'wp_trash_post', '_reset_front_page_settings_for_post' );
diff --git a/wp-includes/post.php b/wp-includes/post.php
index 3940519d4d..1ab71ae53a 100644
--- a/wp-includes/post.php
+++ b/wp-includes/post.php
@@ -398,7 +398,7 @@ function create_initial_post_types() {
 			'show_in_menu'            => false,
 			'show_in_rest'            => true,
 			'rewrite'                 => false,
-			'rest_base'               => 'wp_template',
+			'rest_base'               => 'created-templates',
 			'rest_controller_class'   => 'WP_REST_Posts_Controller',
 			'late_route_registration' => true,
 			'capability_type'         => array( 'template', 'templates' ),
diff --git a/wp-includes/rest-api.php b/wp-includes/rest-api.php
index d23931a589..7e3ed578ec 100644
--- a/wp-includes/rest-api.php
+++ b/wp-includes/rest-api.php
@@ -263,15 +263,6 @@ function rest_api_default_filters() {
  * @since 4.7.0
  */
 function create_initial_rest_routes() {
-	global $wp_post_types;
-
-	// Register the registered templates endpoint. For that we need to copy the
-	// wp_template post type so that it's available as an entity in core-data.
-	$wp_post_types['wp_registered_template']                        = clone $wp_post_types['wp_template'];
-	$wp_post_types['wp_registered_template']->name                  = 'wp_registered_template';
-	$wp_post_types['wp_registered_template']->rest_base             = 'wp_registered_template';
-	$wp_post_types['wp_registered_template']->rest_controller_class = 'WP_REST_Registered_Templates_Controller';
-
 	foreach ( get_post_types( array( 'show_in_rest' => true ), 'objects' ) as $post_type ) {
 		$controller = $post_type->get_rest_controller();
 
@@ -298,11 +289,14 @@ function create_initial_rest_routes() {
 		}
 	}
 
+	global $wp_post_types;
+
 	// Register the old templates endpoints. The WP_REST_Templates_Controller
 	// and sub-controllers used linked to the wp_template post type, but are no
 	// longer. They still require a post type object when contructing the class.
 	// To maintain backward and changes to these controller classes, we make use
 	// that the wp_template post type has the right information it needs.
+	$current_wp_template_rest_base           = $wp_post_types['wp_template']->rest_base;
 	$wp_post_types['wp_template']->rest_base = 'templates';
 	// Store the classes so they can be restored.
 	$original_rest_controller_class           = $wp_post_types['wp_template']->rest_controller_class;
@@ -328,7 +322,7 @@ function create_initial_rest_routes() {
 	$wp_post_types['wp_template']->autosave_rest_controller_class  = $original_autosave_rest_controller_class;
 	$wp_post_types['wp_template']->revisions_rest_controller_class = $original_revisions_rest_controller_class;
 	// Restore the original base.
-	$wp_post_types['wp_template']->rest_base = 'wp_template';
+	$wp_post_types['wp_template']->rest_base = $current_wp_template_rest_base;
 
 	// Register the old routes.
 	$autosaves_controller->register_routes();
@@ -356,6 +350,10 @@ function create_initial_rest_routes() {
 		)
 	);
 
+	// Registered templates.
+	$controller = new WP_REST_Registered_Templates_Controller();
+	$controller->register_routes();
+
 	// Post types.
 	$controller = new WP_REST_Post_Types_Controller();
 	$controller->register_routes();
diff --git a/wp-includes/rest-api/endpoints/class-wp-rest-registered-templates-controller.php b/wp-includes/rest-api/endpoints/class-wp-rest-registered-templates-controller.php
index 97b65af757..fd912bfb45 100644
--- a/wp-includes/rest-api/endpoints/class-wp-rest-registered-templates-controller.php
+++ b/wp-includes/rest-api/endpoints/class-wp-rest-registered-templates-controller.php
@@ -1,6 +1,12 @@
 <?php
 
 class WP_REST_Registered_Templates_Controller extends WP_REST_Templates_Controller {
+	public function __construct() {
+		parent::__construct( 'wp_template' );
+		$this->rest_base = 'registered-templates';
+		$this->namespace = 'wp/v2';
+	}
+
 	public function register_routes() {
 		// Lists all templates.
 		register_rest_route(
@@ -81,9 +87,8 @@ class WP_REST_Registered_Templates_Controller extends WP_REST_Templates_Controll
 		$query_result = get_registered_block_templates( $query );
 		$templates    = array();
 		foreach ( $query_result as $template ) {
-			$item               = $this->prepare_item_for_response( $template, $request );
-			$item->data['type'] = 'wp_registered_template';
-			$templates[]        = $this->prepare_response_for_collection( $item );
+			$item        = $this->prepare_item_for_response( $template, $request );
+			$templates[] = $this->prepare_response_for_collection( $item );
 		}
 
 		return rest_ensure_response( $templates );
@@ -97,8 +102,6 @@ class WP_REST_Registered_Templates_Controller extends WP_REST_Templates_Controll
 		}
 
 		$item = $this->prepare_item_for_response( $template, $request );
-		// adjust the template type here instead
-		$item->data['type'] = 'wp_registered_template';
 		return rest_ensure_response( $item );
 	}
 }
diff --git a/wp-includes/version.php b/wp-includes/version.php
index 25bf53c181..68e18256b5 100644
--- a/wp-includes/version.php
+++ b/wp-includes/version.php
@@ -16,7 +16,7 @@
  *
  * @global string $wp_version
  */
-$wp_version = '6.9-beta1-61077';
+$wp_version = '6.9-beta1-61078';
 
 /**
  * Holds the WordPress DB revision, increments when changes are made to the WordPress DB schema.