diff --git a/src/wp-includes/class-wp-theme-json-resolver.php b/src/wp-includes/class-wp-theme-json-resolver.php
index 5caaf0bb7e1c4..e8c3fa014dc99 100644
--- a/src/wp-includes/class-wp-theme-json-resolver.php
+++ b/src/wp-includes/class-wp-theme-json-resolver.php
@@ -848,6 +848,7 @@ public static function get_style_variations( $scope = 'theme' ) {
 	 * as the value of `_link` object in REST API responses.
 	 *
 	 * @since 6.6.0
+	 * @since 6.7.0 Resolve relative paths in block styles.
 	 *
 	 * @param WP_Theme_JSON $theme_json A theme json instance.
 	 * @return array An array of resolved paths.
@@ -860,21 +861,19 @@ public static function get_resolved_theme_uris( $theme_json ) {
 		}
 
 		$theme_json_data = $theme_json->get_raw_data();
-
-		// Top level styles.
-		$background_image_url = isset( $theme_json_data['styles']['background']['backgroundImage']['url'] ) ? $theme_json_data['styles']['background']['backgroundImage']['url'] : null;
-
 		/*
 		 * The same file convention when registering web fonts.
 		 * See: WP_Font_Face_Resolver::to_theme_file_uri.
 		 */
 		$placeholder = 'file:./';
+
+		// Top level styles.
+		$background_image_url = $theme_json_data['styles']['background']['backgroundImage']['url'] ?? null;
 		if (
 			isset( $background_image_url ) &&
 			is_string( $background_image_url ) &&
 			// Skip if the src doesn't start with the placeholder, as there's nothing to replace.
-			str_starts_with( $background_image_url, $placeholder )
-		) {
+			str_starts_with( $background_image_url, $placeholder ) ) {
 			$file_type          = wp_check_filetype( $background_image_url );
 			$src_url            = str_replace( $placeholder, '', $background_image_url );
 			$resolved_theme_uri = array(
@@ -888,6 +887,33 @@ public static function get_resolved_theme_uris( $theme_json ) {
 			$resolved_theme_uris[] = $resolved_theme_uri;
 		}
 
+		// Block styles.
+		if ( ! empty( $theme_json_data['styles']['blocks'] ) ) {
+			foreach ( $theme_json_data['styles']['blocks'] as $block_name => $block_styles ) {
+				if ( ! isset( $block_styles['background']['backgroundImage']['url'] ) ) {
+					continue;
+				}
+				$background_image_url = $block_styles['background']['backgroundImage']['url'] ?? null;
+				if (
+					isset( $background_image_url ) &&
+					is_string( $background_image_url ) &&
+					// Skip if the src doesn't start with the placeholder, as there's nothing to replace.
+					str_starts_with( $background_image_url, $placeholder ) ) {
+					$file_type          = wp_check_filetype( $background_image_url );
+					$src_url            = str_replace( $placeholder, '', $background_image_url );
+					$resolved_theme_uri = array(
+						'name'   => $background_image_url,
+						'href'   => sanitize_url( get_theme_file_uri( $src_url ) ),
+						'target' => "styles.blocks.{$block_name}.background.backgroundImage.url",
+					);
+					if ( isset( $file_type['type'] ) ) {
+						$resolved_theme_uri['type'] = $file_type['type'];
+					}
+					$resolved_theme_uris[] = $resolved_theme_uri;
+				}
+			}
+		}
+
 		return $resolved_theme_uris;
 	}
 
diff --git a/src/wp-includes/class-wp-theme-json.php b/src/wp-includes/class-wp-theme-json.php
index 63e24340732cf..a72c76c3c9beb 100644
--- a/src/wp-includes/class-wp-theme-json.php
+++ b/src/wp-includes/class-wp-theme-json.php
@@ -520,10 +520,10 @@ class WP_Theme_JSON {
 	 */
 	const VALID_STYLES = array(
 		'background' => array(
-			'backgroundImage'    => 'top',
-			'backgroundPosition' => 'top',
-			'backgroundRepeat'   => 'top',
-			'backgroundSize'     => 'top',
+			'backgroundImage'    => null,
+			'backgroundPosition' => null,
+			'backgroundRepeat'   => null,
+			'backgroundSize'     => null,
 		),
 		'border'     => array(
 			'color'  => null,
diff --git a/src/wp-includes/global-styles-and-settings.php b/src/wp-includes/global-styles-and-settings.php
index b413273a64974..a0c36e9cf4654 100644
--- a/src/wp-includes/global-styles-and-settings.php
+++ b/src/wp-includes/global-styles-and-settings.php
@@ -299,6 +299,7 @@ function wp_get_global_styles_custom_css() {
  * Adds global style rules to the inline style for each block.
  *
  * @since 6.1.0
+ * @since 6.7.0 Resolve relative paths in block styles.
  *
  * @global WP_Styles $wp_styles
  */
@@ -306,6 +307,7 @@ function wp_add_global_styles_for_blocks() {
 	global $wp_styles;
 
 	$tree        = WP_Theme_JSON_Resolver::get_merged_data();
+	$tree        = WP_Theme_JSON_Resolver::resolve_theme_file_uris( $tree );
 	$block_nodes = $tree->get_styles_block_nodes();
 
 	$can_use_cached = ! wp_is_development_mode( 'theme' );