diff --git a/src/wp-includes/rest-api/fields/class-wp-rest-comment-meta-fields.php b/src/wp-includes/rest-api/fields/class-wp-rest-comment-meta-fields.php
index 033ef9cd872f7..0f5f316c594ba 100644
--- a/src/wp-includes/rest-api/fields/class-wp-rest-comment-meta-fields.php
+++ b/src/wp-includes/rest-api/fields/class-wp-rest-comment-meta-fields.php
@@ -16,6 +16,14 @@
  */
 class WP_REST_Comment_Meta_Fields extends WP_REST_Meta_Fields {
 
+	/**
+	 * Cache invalidation callback for comments.
+	 *
+	 * @since 6.9.0
+	 * @var string
+	 */
+	protected $cache_callback = 'wp_cache_set_comments_last_changed';
+
 	/**
 	 * Retrieves the comment type for comment meta.
 	 *
diff --git a/src/wp-includes/rest-api/fields/class-wp-rest-meta-fields.php b/src/wp-includes/rest-api/fields/class-wp-rest-meta-fields.php
index a9c3fbcde831a..d8fa768f44d27 100644
--- a/src/wp-includes/rest-api/fields/class-wp-rest-meta-fields.php
+++ b/src/wp-includes/rest-api/fields/class-wp-rest-meta-fields.php
@@ -15,6 +15,14 @@
 #[AllowDynamicProperties]
 abstract class WP_REST_Meta_Fields {
 
+	/**
+	 * Cache invalidation callback for the object type's last_changed key.
+	 *
+	 * @since 6.9.0
+	 * @var string
+	 */
+	protected $cache_callback = '';
+
 	/**
 	 * Retrieves the object meta type.
 	 *
@@ -143,6 +151,20 @@ public function update_value( $meta, $object_id ) {
 		$fields = $this->get_registered_fields();
 		$error  = new WP_Error();
 
+		/*
+		 * Temporarily unhook the last_changed cache invalidation to avoid
+		 * firing it once per meta key during a batch update.
+		 */
+		$meta_type          = $this->get_meta_type();
+		$has_cache_callback = ! empty( $this->cache_callback )
+			&& function_exists( $this->cache_callback );
+
+		if ( $has_cache_callback ) {
+			remove_action( "added_{$meta_type}_meta", $this->cache_callback );
+			remove_action( "updated_{$meta_type}_meta", $this->cache_callback );
+			remove_action( "deleted_{$meta_type}_meta", $this->cache_callback );
+		}
+
 		foreach ( $fields as $meta_key => $args ) {
 			$name = $args['name'];
 			if ( ! array_key_exists( $name, $meta ) ) {
@@ -212,6 +234,17 @@ public function update_value( $meta, $object_id ) {
 			}
 		}
 
+		/*
+		 * Re-hook the callback and call it once to invalidate the cache
+		 * for the entire batch, rather than once per meta key.
+		 */
+		if ( $has_cache_callback ) {
+			add_action( "added_{$meta_type}_meta", $this->cache_callback );
+			add_action( "updated_{$meta_type}_meta", $this->cache_callback );
+			add_action( "deleted_{$meta_type}_meta", $this->cache_callback );
+			call_user_func( $this->cache_callback );
+		}
+
 		if ( $error->has_errors() ) {
 			return $error;
 		}
diff --git a/src/wp-includes/rest-api/fields/class-wp-rest-post-meta-fields.php b/src/wp-includes/rest-api/fields/class-wp-rest-post-meta-fields.php
index 4b1dc23b30b5f..456221b6350d0 100644
--- a/src/wp-includes/rest-api/fields/class-wp-rest-post-meta-fields.php
+++ b/src/wp-includes/rest-api/fields/class-wp-rest-post-meta-fields.php
@@ -24,6 +24,14 @@ class WP_REST_Post_Meta_Fields extends WP_REST_Meta_Fields {
 	 */
 	protected $post_type;
 
+	/**
+	 * Cache invalidation callback for posts.
+	 *
+	 * @since 6.9.0
+	 * @var string
+	 */
+	protected $cache_callback = 'wp_cache_set_posts_last_changed';
+
 	/**
 	 * Constructor.
 	 *
diff --git a/src/wp-includes/rest-api/fields/class-wp-rest-term-meta-fields.php b/src/wp-includes/rest-api/fields/class-wp-rest-term-meta-fields.php
index 281e1316c9ab0..4e969d80ddc19 100644
--- a/src/wp-includes/rest-api/fields/class-wp-rest-term-meta-fields.php
+++ b/src/wp-includes/rest-api/fields/class-wp-rest-term-meta-fields.php
@@ -24,6 +24,14 @@ class WP_REST_Term_Meta_Fields extends WP_REST_Meta_Fields {
 	 */
 	protected $taxonomy;
 
+	/**
+	 * Cache invalidation callback for terms.
+	 *
+	 * @since 6.9.0
+	 * @var string
+	 */
+	protected $cache_callback = 'wp_cache_set_terms_last_changed';
+
 	/**
 	 * Constructor.
 	 *
diff --git a/src/wp-includes/rest-api/fields/class-wp-rest-user-meta-fields.php b/src/wp-includes/rest-api/fields/class-wp-rest-user-meta-fields.php
index fb1513c58ad4c..6d05095c8aad7 100644
--- a/src/wp-includes/rest-api/fields/class-wp-rest-user-meta-fields.php
+++ b/src/wp-includes/rest-api/fields/class-wp-rest-user-meta-fields.php
@@ -16,6 +16,14 @@
  */
 class WP_REST_User_Meta_Fields extends WP_REST_Meta_Fields {
 
+	/**
+	 * Cache invalidation callback for users.
+	 *
+	 * @since 6.9.0
+	 * @var string
+	 */
+	protected $cache_callback = 'wp_cache_set_users_last_changed';
+
 	/**
 	 * Retrieves the user meta type.
 	 *
diff --git a/tests/phpunit/tests/rest-api/rest-post-meta-fields.php b/tests/phpunit/tests/rest-api/rest-post-meta-fields.php
index 5ce72a57fa55f..3b4908558dd29 100644
--- a/tests/phpunit/tests/rest-api/rest-post-meta-fields.php
+++ b/tests/phpunit/tests/rest-api/rest-post-meta-fields.php
@@ -4014,4 +4014,68 @@ public static function data_scalar_default_values() {
 			'string default'  => array( 'string', 'string', 'string2' ),
 		);
 	}
+
+	/**
+	 * Tests that the cache callback is re-hooked after a batch meta update.
+	 *
+	 * @ticket 65486
+	 */
+	public function test_update_value_batch_rehooks_cache_callback_after_update() {
+		register_meta(
+			'post',
+			'batch_key_1',
+			array(
+				'show_in_rest' => true,
+				'single'       => true,
+				'type'         => 'string',
+			)
+		);
+		register_meta(
+			'post',
+			'batch_key_2',
+			array(
+				'show_in_rest' => true,
+				'single'       => true,
+				'type'         => 'string',
+			)
+		);
+		register_meta(
+			'post',
+			'batch_key_3',
+			array(
+				'show_in_rest' => true,
+				'single'       => true,
+				'type'         => 'string',
+			)
+		);
+
+		global $wp_rest_server;
+		$wp_rest_server = new Spy_REST_Server();
+		do_action( 'rest_api_init', $wp_rest_server );
+
+		$this->grant_write_permission();
+
+		$data    = array(
+			'meta' => array(
+				'batch_key_1' => 'value1',
+				'batch_key_2' => 'value2',
+				'batch_key_3' => 'value3',
+			),
+		);
+		$request = new WP_REST_Request( 'POST', sprintf( '/wp/v2/posts/%d', self::$post_id ) );
+		$request->set_body_params( $data );
+
+		$response = rest_get_server()->dispatch( $request );
+		$this->assertSame( 200, $response->get_status() );
+
+		// Verify meta values were persisted.
+		$this->assertSame( 'value1', get_post_meta( self::$post_id, 'batch_key_1', true ) );
+		$this->assertSame( 'value2', get_post_meta( self::$post_id, 'batch_key_2', true ) );
+		$this->assertSame( 'value3', get_post_meta( self::$post_id, 'batch_key_3', true ) );
+
+		// The cache callback must be re-hooked on all three meta actions.
+		$this->assertNotFalse( has_action( 'added_post_meta', 'wp_cache_set_posts_last_changed' ) );
+		$this->assertNotFalse( has_action( 'updated_post_meta', 'wp_cache_set_posts_last_changed' ) );
+		$this->assertNotFalse( has_action( 'deleted_post_meta', 'wp_cache_set_posts_last_changed' ) );
+	}
 }