diff --git a/src/wp-includes/block-supports/custom-css.php b/src/wp-includes/block-supports/custom-css.php
index 2cd7644ed54b1..d4331ae3706ae 100644
--- a/src/wp-includes/block-supports/custom-css.php
+++ b/src/wp-includes/block-supports/custom-css.php
@@ -12,17 +12,28 @@
  *
  * @param array $parsed_block The parsed block.
  * @return array The same parsed block with custom CSS class name added if appropriate.
+ *
+ * @phpstan-param array{
+ *     blockName: string|null,
+ *     attrs: array{
+ *         className?: string,
+ *         style?: array{
+ *             css?: string,
+ *             ...
+ *         },
+ *         ...
+ *     },
+ *     ...
+ * } $parsed_block
  */
 function wp_render_custom_css_support_styles( $parsed_block ) {
-	$block_type = WP_Block_Type_Registry::get_instance()->get_registered( $parsed_block['blockName'] );
-
-	if ( ! block_has_support( $block_type, 'customCSS', true ) ) {
+	$custom_css = $parsed_block['attrs']['style']['css'] ?? null;
+	if ( ! is_string( $custom_css ) || '' === trim( $custom_css ) ) {
 		return $parsed_block;
 	}
 
-	$custom_css = trim( $parsed_block['attrs']['style']['css'] ?? '' );
-
-	if ( empty( $custom_css ) ) {
+	$block_type = WP_Block_Type_Registry::get_instance()->get_registered( $parsed_block['blockName'] );
+	if ( ! block_has_support( $block_type, 'customCSS', true ) ) {
 		return $parsed_block;
 	}
 
@@ -32,9 +43,10 @@ function wp_render_custom_css_support_styles( $parsed_block ) {
 	}
 
 	// Generate a unique class name for this block instance.
-	$class_name         = wp_unique_id_from_values( $parsed_block, 'wp-custom-css-' );
-	$updated_class_name = isset( $parsed_block['attrs']['className'] )
-		? $parsed_block['attrs']['className'] . " $class_name"
+	$class_name          = wp_unique_id_from_values( $parsed_block, 'wp-custom-css-' );
+	$existing_class_name = $parsed_block['attrs']['className'] ?? null;
+	$updated_class_name  = is_string( $existing_class_name )
+		? "$existing_class_name $class_name"
 		: $class_name;
 
 	_wp_array_set( $parsed_block, array( 'attrs', 'className' ), $updated_class_name );
@@ -68,7 +80,7 @@ function wp_enqueue_block_custom_css() {
 /**
  * Applies the custom CSS class name to the block's rendered HTML.
  *
- * The class name is generated in `wp_render_custom_css_support_styles`
+ * The class name is generated in {@see wp_render_custom_css_support_styles()}
  * and stored in block attributes. This filter adds it to the actual markup.
  *
  * @since 7.0.0
@@ -76,12 +88,34 @@ function wp_enqueue_block_custom_css() {
  * @param string $block_content Rendered block content.
  * @param array  $block         Block object.
  * @return string               Filtered block content.
+ *
+ * @phpstan-param array{
+ *     attrs: array{
+ *         className?: string,
+ *         ...
+ *     },
+ *     ...
+ * } $block
  */
 function wp_render_custom_css_class_name( $block_content, $block ) {
-	$class_string = $block['attrs']['className'] ?? '';
-	preg_match( '/\bwp-custom-css-\S+\b/', $class_string, $matches );
+	$class_name_attr = $block['attrs']['className'] ?? null;
+
+	if ( ! is_string( $class_name_attr ) || ! str_contains( $class_name_attr, 'wp-custom-css-' ) ) {
+		return $block_content;
+	}
 
-	if ( empty( $matches ) ) {
+	// Parse out the 'wp-custom-css-*' class name added by wp_render_custom_css_support_styles().
+	$custom_class_name = null;
+	$token_delimiter   = " \t\f\r\n";
+	$class_token       = strtok( $class_name_attr, $token_delimiter );
+	while ( false !== $class_token ) {
+		if ( str_starts_with( $class_token, 'wp-custom-css-' ) ) {
+			$custom_class_name = $class_token;
+			break;
+		}
+		$class_token = strtok( $token_delimiter );
+	}
+	if ( null === $custom_class_name ) {
 		return $block_content;
 	}
 
@@ -89,7 +123,7 @@ function wp_render_custom_css_class_name( $block_content, $block ) {
 
 	if ( $tags->next_tag() ) {
 		$tags->add_class( 'has-custom-css' );
-		$tags->add_class( $matches[0] );
+		$tags->add_class( $custom_class_name );
 	}
 
 	return $tags->get_updated_html();
diff --git a/src/wp-includes/blocks.php b/src/wp-includes/blocks.php
index cc1ac60667773..6a6418d966457 100644
--- a/src/wp-includes/blocks.php
+++ b/src/wp-includes/blocks.php
@@ -2604,9 +2604,9 @@ function unregister_block_style( $block_name, $block_style_name ) {
  * @since 5.8.0
  * @since 6.4.0 The `$feature` parameter now supports a string.
  *
- * @param WP_Block_Type $block_type    Block type to check for support.
- * @param string|array  $feature       Feature slug, or path to a specific feature to check support for.
- * @param mixed         $default_value Optional. Fallback value for feature support. Default false.
+ * @param WP_Block_Type|null $block_type    Block type to check for support.
+ * @param string|array       $feature       Feature slug, or path to a specific feature to check support for.
+ * @param mixed              $default_value Optional. Fallback value for feature support. Default false.
  * @return bool Whether the feature is supported.
  */
 function block_has_support( $block_type, $feature, $default_value = false ) {
diff --git a/src/wp-includes/html-api/class-wp-html-tag-processor.php b/src/wp-includes/html-api/class-wp-html-tag-processor.php
index 8397ecf520fa2..4015b352c153c 100644
--- a/src/wp-includes/html-api/class-wp-html-tag-processor.php
+++ b/src/wp-includes/html-api/class-wp-html-tag-processor.php
@@ -1175,6 +1175,8 @@ public function paused_at_incomplete_token(): bool {
 	 *     // Outputs: "free <egg> lang-en "
 	 *
 	 * @since 6.4.0
+	 *
+	 * @return Generator<int, non-empty-string>
 	 */
 	public function class_list() {
 		if ( self::STATE_MATCHED_TAG !== $this->parser_state ) {
diff --git a/tests/phpunit/tests/block-supports/wpRenderCustomCssClassName.php b/tests/phpunit/tests/block-supports/wpRenderCustomCssClassName.php
index 0bcbc6c708468..1247ca65a1a33 100644
--- a/tests/phpunit/tests/block-supports/wpRenderCustomCssClassName.php
+++ b/tests/phpunit/tests/block-supports/wpRenderCustomCssClassName.php
@@ -29,9 +29,18 @@ public function test_adds_class_to_content( $block_content, $block, $expected_cl
 	/**
 	 * Data provider.
 	 *
-	 * @return array
+	 * @return array<string, array{
+	 *     block_content: string,
+	 *     block: array{
+	 *         blockName: string,
+	 *         attrs: array{
+	 *             className: string,
+	 *         },
+	 *     },
+	 *     expected_class: string,
+	 * }>
 	 */
-	public function data_adds_class_to_content() {
+	public function data_adds_class_to_content(): array {
 		return array(
 			'class is added to block content'           => array(
 				'block_content'  => '<div class="wp-block-paragraph">Test content</div>',
@@ -53,6 +62,16 @@ public function data_adds_class_to_content() {
 				),
 				'expected_class' => 'wp-custom-css-mixed123',
 			),
+			'class between whitespace is added'         => array(
+				'block_content'  => '<div class="wp-block-paragraph">Test content</div>',
+				'block'          => array(
+					'blockName' => 'core/paragraph',
+					'attrs'     => array(
+						'className' => "\twp-custom-css-123abc\t",
+					),
+				),
+				'expected_class' => 'wp-custom-css-123abc',
+			),
 		);
 	}
 
@@ -113,6 +132,15 @@ public function data_returns_unchanged_content() {
 					),
 				),
 			),
+			'prefixed custom CSS class'     => array(
+				'block_content' => '<div class="wp-block-paragraph">Test content</div>',
+				'block'         => array(
+					'blockName' => 'core/paragraph',
+					'attrs'     => array(
+						'className' => 'my-wp-custom-css-456def',
+					),
+				),
+			),
 			'className is not set in attrs' => array(
 				'block_content' => '<div class="wp-block-paragraph">Test content</div>',
 				'block'         => array(