diff --git a/wp-includes/class-wp-query.php b/wp-includes/class-wp-query.php
index e6a3e6b743..f683a52bd1 100644
--- a/wp-includes/class-wp-query.php
+++ b/wp-includes/class-wp-query.php
@@ -1027,7 +1027,7 @@ class WP_Query {
 		}
 
 		if ( ! ( $this->is_singular || $this->is_archive || $this->is_search || $this->is_feed
-				|| ( defined( 'REST_REQUEST' ) && REST_REQUEST && $this->is_main_query() )
+				|| ( wp_is_serving_rest_request() && $this->is_main_query() )
 				|| $this->is_trackback || $this->is_404 || $this->is_admin || $this->is_robots || $this->is_favicon ) ) {
 			$this->is_home = true;
 		}
diff --git a/wp-includes/deprecated.php b/wp-includes/deprecated.php
index e63708f91b..ec7b33f360 100644
--- a/wp-includes/deprecated.php
+++ b/wp-includes/deprecated.php
@@ -5436,7 +5436,7 @@ function _wp_theme_json_webfonts_handler() {
 		$settings = WP_Theme_JSON_Resolver::get_merged_data()->get_settings();
 
 		// If in the editor, add webfonts defined in variations.
-		if ( is_admin() || ( defined( 'REST_REQUEST' ) && REST_REQUEST ) ) {
+		if ( is_admin() || wp_is_rest_endpoint() ) {
 			$variations = WP_Theme_JSON_Resolver::get_style_variations();
 			foreach ( $variations as $variation ) {
 				// Skip if fontFamilies are not defined in the variation.
diff --git a/wp-includes/functions.php b/wp-includes/functions.php
index a3a5e56bfa..ff55251d7d 100644
--- a/wp-includes/functions.php
+++ b/wp-includes/functions.php
@@ -3718,7 +3718,7 @@ function wp_die( $message = '', $title = '', $args = array() ) {
 		 * @param callable $callback Callback function name.
 		 */
 		$callback = apply_filters( 'wp_die_json_handler', '_json_wp_die_handler' );
-	} elseif ( defined( 'REST_REQUEST' ) && REST_REQUEST && wp_is_jsonp_request() ) {
+	} elseif ( wp_is_serving_rest_request() && wp_is_jsonp_request() ) {
 		/**
 		 * Filters the callback for killing WordPress execution for JSONP REST requests.
 		 *
@@ -4441,7 +4441,7 @@ function _wp_json_prepare_data( $value ) {
  * @param int   $flags       Optional. Options to be passed to json_encode(). Default 0.
  */
 function wp_send_json( $response, $status_code = null, $flags = 0 ) {
-	if ( defined( 'REST_REQUEST' ) && REST_REQUEST ) {
+	if ( wp_is_serving_rest_request() ) {
 		_doing_it_wrong(
 			__FUNCTION__,
 			sprintf(
@@ -4697,6 +4697,23 @@ function _mce_set_direction( $mce_init ) {
 	return $mce_init;
 }
 
+/**
+ * Determines whether WordPress is currently serving a REST API request.
+ *
+ * The function relies on the 'REST_REQUEST' global. As such, it only returns true when an actual REST _request_ is
+ * being made. It does not return true when a REST endpoint is hit as part of another request, e.g. for preloading a
+ * REST response. See {@see wp_is_rest_endpoint()} for that purpose.
+ *
+ * This function should not be called until the {@see 'parse_request'} action, as the constant is only defined then,
+ * even for an actual REST request.
+ *
+ * @since 6.5.0
+ *
+ * @return bool True if it's a WordPress REST API request, false otherwise.
+ */
+function wp_is_serving_rest_request() {
+	return defined( 'REST_REQUEST' ) && REST_REQUEST;
+}
 
 /**
  * Converts smiley code to the icon graphic file equivalent.
diff --git a/wp-includes/load.php b/wp-includes/load.php
index 520902cdd6..0dbbc187cf 100644
--- a/wp-includes/load.php
+++ b/wp-includes/load.php
@@ -598,6 +598,10 @@ function wp_debug_mode() {
 		error_reporting( E_CORE_ERROR | E_CORE_WARNING | E_COMPILE_ERROR | E_ERROR | E_WARNING | E_PARSE | E_USER_ERROR | E_USER_WARNING | E_RECOVERABLE_ERROR );
 	}
 
+	/*
+	 * The 'REST_REQUEST' check here is optimistic as the constant is most
+	 * likely not set at this point even if it is in fact a REST request.
+	 */
 	if ( defined( 'XMLRPC_REQUEST' ) || defined( 'REST_REQUEST' ) || defined( 'MS_FILES_REQUEST' )
 		|| ( defined( 'WP_INSTALLING' ) && WP_INSTALLING )
 		|| wp_doing_ajax() || wp_is_json_request()
diff --git a/wp-includes/rest-api.php b/wp-includes/rest-api.php
index 61e324e801..2631a6663f 100644
--- a/wp-includes/rest-api.php
+++ b/wp-includes/rest-api.php
@@ -209,7 +209,7 @@ function rest_api_register_rewrites() {
  * @since 4.4.0
  */
 function rest_api_default_filters() {
-	if ( defined( 'REST_REQUEST' ) && REST_REQUEST ) {
+	if ( wp_is_serving_rest_request() ) {
 		// Deprecated reporting.
 		add_action( 'deprecated_function_run', 'rest_handle_deprecated_function', 10, 3 );
 		add_filter( 'deprecated_function_trigger_error', '__return_false' );
@@ -3389,3 +3389,38 @@ function rest_convert_error_to_response( $error ) {
 
 	return new WP_REST_Response( $data, $status );
 }
+
+/**
+ * Checks whether a REST API endpoint request is currently being handled.
+ *
+ * This may be a standalone REST API request, or an internal request dispatched from within a regular page load.
+ *
+ * @since 6.5.0
+ *
+ * @global WP_REST_Server $wp_rest_server REST server instance.
+ *
+ * @return bool True if a REST endpoint request is currently being handled, false otherwise.
+ */
+function wp_is_rest_endpoint() {
+	/* @var WP_REST_Server $wp_rest_server */
+	global $wp_rest_server;
+
+	// Check whether this is a standalone REST request.
+	$is_rest_endpoint = wp_is_serving_rest_request();
+	if ( ! $is_rest_endpoint ) {
+		// Otherwise, check whether an internal REST request is currently being handled.
+		$is_rest_endpoint = isset( $wp_rest_server )
+			&& $wp_rest_server->is_dispatching();
+	}
+
+	/**
+	 * Filters whether a REST endpoint request is currently being handled.
+	 *
+	 * This may be a standalone REST API request, or an internal request dispatched from within a regular page load.
+	 *
+	 * @since 6.5.0
+	 *
+	 * @param bool $is_request_endpoint Whether a REST endpoint request is currently being handled.
+	 */
+	return (bool) apply_filters( 'wp_is_rest_endpoint', $is_rest_endpoint );
+}
diff --git a/wp-includes/rest-api/class-wp-rest-server.php b/wp-includes/rest-api/class-wp-rest-server.php
index 6838579ce8..861f5115e6 100644
--- a/wp-includes/rest-api/class-wp-rest-server.php
+++ b/wp-includes/rest-api/class-wp-rest-server.php
@@ -87,6 +87,14 @@ class WP_REST_Server {
 	 */
 	protected $embed_cache = array();
 
+	/**
+	 * Stores request objects that are currently being handled.
+	 *
+	 * @since 6.5.0
+	 * @var array
+	 */
+	protected $dispatching_requests = array();
+
 	/**
 	 * Instantiates the REST server.
 	 *
@@ -983,6 +991,8 @@ class WP_REST_Server {
 	 * @return WP_REST_Response Response returned by the callback.
 	 */
 	public function dispatch( $request ) {
+		$this->dispatching_requests[] = $request;
+
 		/**
 		 * Filters the pre-calculated result of a REST API dispatch request.
 		 *
@@ -1008,6 +1018,7 @@ class WP_REST_Server {
 				$result = $this->error_to_response( $result );
 			}
 
+			array_pop( $this->dispatching_requests );
 			return $result;
 		}
 
@@ -1015,7 +1026,9 @@ class WP_REST_Server {
 		$matched = $this->match_request_to_handler( $request );
 
 		if ( is_wp_error( $matched ) ) {
-			return $this->error_to_response( $matched );
+			$response = $this->error_to_response( $matched );
+			array_pop( $this->dispatching_requests );
+			return $response;
 		}
 
 		list( $route, $handler ) = $matched;
@@ -1040,7 +1053,22 @@ class WP_REST_Server {
 			}
 		}
 
-		return $this->respond_to_request( $request, $route, $handler, $error );
+		$response = $this->respond_to_request( $request, $route, $handler, $error );
+		array_pop( $this->dispatching_requests );
+		return $response;
+	}
+
+	/**
+	 * Returns whether the REST server is currently dispatching / responding to a request.
+	 *
+	 * This may be a standalone REST API request, or an internal request dispatched from within a regular page load.
+	 *
+	 * @since 6.5.0
+	 *
+	 * @return bool Whether the REST server is currently handling a request.
+	 */
+	public function is_dispatching() {
+		return (bool) $this->dispatching_requests;
 	}
 
 	/**
diff --git a/wp-includes/rest-api/endpoints/class-wp-rest-attachments-controller.php b/wp-includes/rest-api/endpoints/class-wp-rest-attachments-controller.php
index 7367c0fc57..c7da6d068b 100644
--- a/wp-includes/rest-api/endpoints/class-wp-rest-attachments-controller.php
+++ b/wp-includes/rest-api/endpoints/class-wp-rest-attachments-controller.php
@@ -201,7 +201,7 @@ class WP_REST_Attachments_Controller extends WP_REST_Posts_Controller {
 
 		wp_after_insert_post( $attachment, false, null );
 
-		if ( defined( 'REST_REQUEST' ) && REST_REQUEST ) {
+		if ( wp_is_serving_rest_request() ) {
 			/*
 			 * Set a custom header with the attachment_id.
 			 * Used by the browser/client to resume creating image sub-sizes after a PHP fatal error.
@@ -630,7 +630,7 @@ class WP_REST_Attachments_Controller extends WP_REST_Posts_Controller {
 			update_post_meta( $new_attachment_id, '_wp_attachment_image_alt', wp_slash( $image_alt ) );
 		}
 
-		if ( defined( 'REST_REQUEST' ) && REST_REQUEST ) {
+		if ( wp_is_serving_rest_request() ) {
 			/*
 			 * Set a custom header with the attachment_id.
 			 * Used by the browser/client to resume creating image sub-sizes after a PHP fatal error.
diff --git a/wp-includes/rest-api/endpoints/class-wp-rest-url-details-controller.php b/wp-includes/rest-api/endpoints/class-wp-rest-url-details-controller.php
index c9ac6675d0..7dcc4d7923 100644
--- a/wp-includes/rest-api/endpoints/class-wp-rest-url-details-controller.php
+++ b/wp-includes/rest-api/endpoints/class-wp-rest-url-details-controller.php
@@ -128,7 +128,7 @@ class WP_REST_URL_Details_Controller extends WP_REST_Controller {
 	 *
 	 * @since 5.9.0
 	 *
-	 * @param WP_REST_REQUEST $request Full details about the request.
+	 * @param WP_REST_Request $request Full details about the request.
 	 * @return WP_REST_Response|WP_Error The parsed details as a response object. WP_Error if there are errors.
 	 */
 	public function parse_url_details( $request ) {
diff --git a/wp-includes/script-loader.php b/wp-includes/script-loader.php
index 8886cb587b..6425afe874 100644
--- a/wp-includes/script-loader.php
+++ b/wp-includes/script-loader.php
@@ -2586,7 +2586,7 @@ function wp_should_load_block_editor_scripts_and_styles() {
  * @return bool Whether separate assets will be loaded.
  */
 function wp_should_load_separate_core_block_assets() {
-	if ( is_admin() || is_feed() || ( defined( 'REST_REQUEST' ) && REST_REQUEST ) ) {
+	if ( is_admin() || is_feed() || wp_is_rest_endpoint() ) {
 		return false;
 	}
 
diff --git a/wp-includes/user.php b/wp-includes/user.php
index 5dbff2b929..5d8cd9f57c 100644
--- a/wp-includes/user.php
+++ b/wp-includes/user.php
@@ -333,6 +333,7 @@ function wp_authenticate_application_password( $input_user, $username, $password
 		return $input_user;
 	}
 
+	// The 'REST_REQUEST' check here may happen too early for the constant to be available.
 	$is_api_request = ( ( defined( 'XMLRPC_REQUEST' ) && XMLRPC_REQUEST ) || ( defined( 'REST_REQUEST' ) && REST_REQUEST ) );
 
 	/**
diff --git a/wp-includes/version.php b/wp-includes/version.php
index 9e43c965d3..205deb7271 100644
--- a/wp-includes/version.php
+++ b/wp-includes/version.php
@@ -16,7 +16,7 @@
  *
  * @global string $wp_version
  */
-$wp_version = '6.5-alpha-57311';
+$wp_version = '6.5-alpha-57312';
 
 /**
  * Holds the WordPress DB revision, increments when changes are made to the WordPress DB schema.