diff --git a/lib/compat/wordpress-5.9/default-theme-supports.php b/lib/compat/wordpress-5.9/default-theme-supports.php
index 84df5ca0d91c47..5328fc4625c6fb 100644
--- a/lib/compat/wordpress-5.9/default-theme-supports.php
+++ b/lib/compat/wordpress-5.9/default-theme-supports.php
@@ -19,3 +19,59 @@
 	add_theme_support( 'automatic-feed-links' );
 	add_filter( 'should_load_separate_core_block_assets', '__return_true' );
 }
+
+/**
+ * Overrides the WordPress enqueue_block_styles_assets function, which contains
+ * a bug eventually leading to a fatal error for full site editing enabled themes
+ * which do register custom block styles and don't have a template for requested
+ * template (eg.: 404)
+ *
+ * More details on the bug can be found in: https://core.trac.wordpress.org/ticket/54323
+ *
+ * @see enqueue_block_styles_assets
+ */
+function gutenberg_enqueue_block_styles_assets() {
+	$block_styles = WP_Block_Styles_Registry::get_instance()->get_all_registered();
+
+	foreach ( $block_styles as $block_name => $styles ) {
+		foreach ( $styles as $style_properties ) {
+			if ( isset( $style_properties['style_handle'] ) ) {
+
+				// If the site loads separate styles per-block, enqueue the stylesheet on render.
+				if ( wp_should_load_separate_core_block_assets() ) {
+					add_filter(
+						'render_block',
+						function( $html ) use ( $style_properties ) {
+							wp_enqueue_style( $style_properties['style_handle'] );
+							return $html;
+						}
+					);
+				} else {
+					wp_enqueue_style( $style_properties['style_handle'] );
+				}
+			}
+			if ( isset( $style_properties['inline_style'] ) ) {
+
+				// Default to "wp-block-library".
+				$handle = 'wp-block-library';
+
+				// If the site loads separate styles per-block, check if the block has a stylesheet registered.
+				if ( wp_should_load_separate_core_block_assets() ) {
+					$block_stylesheet_handle = generate_block_asset_handle( $block_name, 'style' );
+					global $wp_styles;
+					if ( isset( $wp_styles->registered[ $block_stylesheet_handle ] ) ) {
+						$handle = $block_stylesheet_handle;
+					}
+				}
+
+				// Add inline styles to the calculated handle.
+				wp_add_inline_style( $handle, $style_properties['inline_style'] );
+			}
+		}
+	}
+}
+
+if ( version_compare( get_bloginfo( 'version' ), '5.8.2', '<' ) && 30 === has_action( 'enqueue_block_assets', 'enqueue_block_styles_assets' ) ) {
+	remove_action( 'enqueue_block_assets', 'enqueue_block_styles_assets', 30 );
+	add_action( 'enqueue_block_assets', 'gutenberg_enqueue_block_styles_assets', 30 );
+}