diff --git a/wp-includes/class-wp-theme-json.php b/wp-includes/class-wp-theme-json.php
index 15780efc346..5570cd96040 100644
--- a/wp-includes/class-wp-theme-json.php
+++ b/wp-includes/class-wp-theme-json.php
@@ -1439,9 +1439,16 @@ public function get_stylesheet( $types = array( 'variables', 'styles', 'presets'
 	protected function process_blocks_custom_css( $css, $selector ) {
 		$processed_css = '';
 
+		if ( empty( $css ) ) {
+			return $processed_css;
+		}
+
 		// Split CSS nested rules.
 		$parts = explode( '&', $css );
 		foreach ( $parts as $part ) {
+			if ( empty( $part ) ) {
+				continue;
+			}
 			$is_root_css = ( ! str_contains( $part, '{' ) );
 			if ( $is_root_css ) {
 				// If the part doesn't contain braces, it applies to the root level.
@@ -1454,11 +1461,25 @@ protected function process_blocks_custom_css( $css, $selector ) {
 				}
 				$nested_selector = $part[0];
 				$css_value       = $part[1];
-				$part_selector   = str_starts_with( $nested_selector, ' ' )
+
+				/*
+				 * Handle pseudo elements such as ::before, ::after etc. Regex will also
+				 * capture any leading combinator such as >, +, or ~, as well as spaces.
+				 * This allows pseudo elements as descendants e.g. `.parent ::before`.
+				 */
+				$matches            = array();
+				$has_pseudo_element = preg_match( '/([>+~\s]*::[a-zA-Z-]+)/', $nested_selector, $matches );
+				$pseudo_part        = $has_pseudo_element ? $matches[1] : '';
+				$nested_selector    = $has_pseudo_element ? str_replace( $pseudo_part, '', $nested_selector ) : $nested_selector;
+
+				// Finalize selector and re-append pseudo element if required.
+				$part_selector  = str_starts_with( $nested_selector, ' ' )
 					? static::scope_selector( $selector, $nested_selector )
 					: static::append_to_selector( $selector, $nested_selector );
-				$final_selector  = ":root :where($part_selector)";
-				$processed_css  .= $final_selector . '{' . trim( $css_value ) . '}';}
+				$final_selector = ":root :where($part_selector)$pseudo_part";
+
+				$processed_css .= $final_selector . '{' . trim( $css_value ) . '}';
+			}
 		}
 		return $processed_css;
 	}
diff --git a/wp-includes/version.php b/wp-includes/version.php
index 8acea37f6e2..a345d19eba6 100644
--- a/wp-includes/version.php
+++ b/wp-includes/version.php
@@ -16,7 +16,7 @@
  *
  * @global string $wp_version
  */
-$wp_version = '6.6.2-alpha-58986';
+$wp_version = '6.6.2-alpha-58987';
 
 /**
  * Holds the WordPress DB revision, increments when changes are made to the WordPress DB schema.