diff --git a/src/wp-includes/class-wp-theme-json.php b/src/wp-includes/class-wp-theme-json.php
index 5abd2817b8aa4..c2eef1f6e2d5d 100644
--- a/src/wp-includes/class-wp-theme-json.php
+++ b/src/wp-includes/class-wp-theme-json.php
@@ -3216,7 +3216,12 @@ static function ( $pseudo_selector ) use ( $selector ) {
 
 		// 7. Generate and append any custom CSS rules.
 		if ( isset( $node['css'] ) && ! $is_root_selector ) {
-			$block_rules .= $this->process_blocks_custom_css( $node['css'], $selector );
+			$css_feature_selector = $block_metadata['selectors']['css'] ?? null;
+			if ( is_array( $css_feature_selector ) ) {
+				$css_feature_selector = $css_feature_selector['root'] ?? null;
+			}
+			$css_selector = is_string( $css_feature_selector ) ? $css_feature_selector : $selector;
+			$block_rules .= $this->process_blocks_custom_css( $node['css'], $css_selector );
 		}
 
 		return $block_rules;
@@ -4610,10 +4615,10 @@ protected function get_feature_declarations_for_node( $metadata, &$node ) {
 
 		foreach ( $metadata['selectors'] as $feature => $feature_selectors ) {
 			/*
-			 * Skip if this is the block's root selector or the block doesn't
-			 * have any styles for the feature.
+			 * Skip if this is the block's root selector, the custom CSS
+			 * selector, or the block doesn't have any styles for the feature.
 			 */
-			if ( 'root' === $feature || empty( $node[ $feature ] ) ) {
+			if ( 'root' === $feature || 'css' === $feature || empty( $node[ $feature ] ) ) {
 				continue;
 			}
 
diff --git a/tests/phpunit/tests/theme/wpThemeJson.php b/tests/phpunit/tests/theme/wpThemeJson.php
index 95de67c69f98c..6ed1f23d8e5b2 100644
--- a/tests/phpunit/tests/theme/wpThemeJson.php
+++ b/tests/phpunit/tests/theme/wpThemeJson.php
@@ -7054,4 +7054,113 @@ public function test_sanitize_preserves_null_schema_behavior() {
 		$this->assertSame( 'string-value', $settings['appearanceTools'], 'Appearance tools should be string value' );
 		$this->assertSame( array( 'nested' => 'value' ), $settings['custom'], 'Custom should be array value' );
 	}
+
+	/**
+	 * Tests that block custom CSS uses the css feature selector when defined
+	 * in block metadata selectors config.
+	 *
+	 * @ticket 64695
+	 */
+	public function test_get_styles_for_block_custom_css_uses_css_feature_selector() {
+		$theme_json = new WP_Theme_JSON(
+			array(
+				'version' => WP_Theme_JSON::LATEST_SCHEMA,
+				'styles'  => array(
+					'blocks' => array(
+						'core/paragraph' => array(
+							'css' => 'color:red;',
+						),
+					),
+				),
+			)
+		);
+
+		$paragraph_node = array(
+			'name'      => 'core/paragraph',
+			'path'      => array( 'styles', 'blocks', 'core/paragraph' ),
+			'selector'  => 'p',
+			'selectors' => array(
+				'root' => 'p',
+				'css'  => '.custom-p',
+			),
+		);
+
+		$this->assertSame(
+			':root :where(.custom-p){color:red;}',
+			$theme_json->get_styles_for_block( $paragraph_node )
+		);
+	}
+
+	/**
+	 * Tests that block custom CSS falls back to the root selector when no
+	 * css feature selector is defined in block metadata selectors config.
+	 *
+	 * @ticket 64695
+	 */
+	public function test_get_styles_for_block_custom_css_falls_back_to_root_selector() {
+		$theme_json = new WP_Theme_JSON(
+			array(
+				'version' => WP_Theme_JSON::LATEST_SCHEMA,
+				'styles'  => array(
+					'blocks' => array(
+						'core/paragraph' => array(
+							'css' => 'color:red;',
+						),
+					),
+				),
+			)
+		);
+
+		$paragraph_node = array(
+			'name'      => 'core/paragraph',
+			'path'      => array( 'styles', 'blocks', 'core/paragraph' ),
+			'selector'  => 'p',
+			'selectors' => array(
+				'root' => 'p',
+			),
+		);
+
+		$this->assertSame(
+			':root :where(p){color:red;}',
+			$theme_json->get_styles_for_block( $paragraph_node )
+		);
+	}
+
+	/**
+	 * Tests that block custom CSS uses the css feature selector when defined
+	 * as an object with a root subkey in block metadata selectors config.
+	 *
+	 * @ticket 64695
+	 */
+	public function test_get_styles_for_block_custom_css_uses_css_feature_selector_object_form() {
+		$theme_json = new WP_Theme_JSON(
+			array(
+				'version' => WP_Theme_JSON::LATEST_SCHEMA,
+				'styles'  => array(
+					'blocks' => array(
+						'core/paragraph' => array(
+							'css' => 'color:red;',
+						),
+					),
+				),
+			)
+		);
+
+		$paragraph_node = array(
+			'name'      => 'core/paragraph',
+			'path'      => array( 'styles', 'blocks', 'core/paragraph' ),
+			'selector'  => 'p',
+			'selectors' => array(
+				'root' => 'p',
+				'css'  => array(
+					'root' => '.custom-p',
+				),
+			),
+		);
+
+		$this->assertSame(
+			':root :where(.custom-p){color:red;}',
+			$theme_json->get_styles_for_block( $paragraph_node )
+		);
+	}
 }