diff --git a/src/wp-includes/block-editor.php b/src/wp-includes/block-editor.php
index af873178eb7aa..18152756d5b73 100644
--- a/src/wp-includes/block-editor.php
+++ b/src/wp-includes/block-editor.php
@@ -658,6 +658,8 @@ function get_block_editor_settings( array $custom_settings, $block_editor_contex
 		$editor_settings = apply_filters_deprecated( 'block_editor_settings', array( $editor_settings, $post ), '5.8.0', 'block_editor_settings_all' );
 	}
 
+	$editor_settings['canEditCSS'] = current_user_can( 'edit_css' );
+
 	return $editor_settings;
 }
 
diff --git a/src/wp-includes/block-supports/custom-css.php b/src/wp-includes/block-supports/custom-css.php
new file mode 100644
index 0000000000000..9d5b13426f4ef
--- /dev/null
+++ b/src/wp-includes/block-supports/custom-css.php
@@ -0,0 +1,133 @@
+<?php
+/**
+ * Custom CSS block support.
+ *
+ * @package WordPress
+ */
+
+/**
+ * Render the custom CSS stylesheet and add class name to block as required.
+ *
+ * @since 7.0.0
+ *
+ * @param array $parsed_block The parsed block.
+ * @return array The same parsed block with custom CSS class name added if appropriate.
+ */
+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 ) ) {
+		return $parsed_block;
+	}
+
+	$custom_css = trim( $parsed_block['attrs']['style']['css'] ?? '' );
+
+	if ( empty( $custom_css ) ) {
+		return $parsed_block;
+	}
+
+	// Validate CSS doesn't contain HTML markup (same validation as global styles REST API).
+	if ( preg_match( '#</?\w+#', $custom_css ) ) {
+		return $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_array_set( $parsed_block, array( 'attrs', 'className' ), $updated_class_name );
+
+	// Process the custom CSS using the same method as global styles.
+	$selector      = '.' . $class_name;
+	$processed_css = WP_Theme_JSON::process_blocks_custom_css( $custom_css, $selector );
+
+	if ( ! empty( $processed_css ) ) {
+		/*
+		 * Register and add inline style for block custom CSS.
+		 * The style depends on global-styles to ensure custom CSS loads after
+		 * and can override global styles.
+		 */
+		wp_register_style( 'wp-block-custom-css', false, array( 'global-styles' ) );
+		wp_add_inline_style( 'wp-block-custom-css', $processed_css );
+	}
+
+	return $parsed_block;
+}
+
+/**
+ * Enqueues the block custom CSS styles.
+ *
+ * @since 7.0.0
+ */
+function wp_enqueue_block_custom_css() {
+	wp_enqueue_style( 'wp-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`
+ * and stored in block attributes. This filter adds it to the actual markup.
+ *
+ * @since 7.0.0
+ *
+ * @param string $block_content Rendered block content.
+ * @param array  $block         Block object.
+ * @return string               Filtered block content.
+ */
+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 );
+
+	if ( empty( $matches ) ) {
+		return $block_content;
+	}
+
+	$tags = new WP_HTML_Tag_Processor( $block_content );
+
+	if ( $tags->next_tag() ) {
+		$tags->add_class( 'has-custom-css' );
+		$tags->add_class( $matches[0] );
+	}
+
+	return $tags->get_updated_html();
+}
+
+add_filter( 'render_block', 'wp_render_custom_css_class_name', 10, 2 );
+add_filter( 'render_block_data', 'wp_render_custom_css_support_styles', 10, 1 );
+add_action( 'wp_enqueue_scripts', 'wp_enqueue_block_custom_css', 1 );
+
+/**
+ * Registers the style block attribute for block types that support it.
+ *
+ * @param WP_Block_Type $block_type Block Type.
+ */
+function wp_register_custom_css_support( $block_type ) {
+	// Setup attributes and styles within that if needed.
+	if ( ! $block_type->attributes ) {
+		$block_type->attributes = array();
+	}
+
+	// Check for existing style attribute definition e.g. from block.json.
+	if ( array_key_exists( 'style', $block_type->attributes ) ) {
+		return;
+	}
+
+	$has_custom_css_support = block_has_support( $block_type, array( 'customCSS' ), true );
+
+	if ( $has_custom_css_support ) {
+		$block_type->attributes['style'] = array(
+			'type' => 'object',
+		);
+	}
+}
+
+// Register the block support.
+WP_Block_Supports::get_instance()->register(
+	'custom-css',
+	array(
+		'register_attribute' => 'wp_register_custom_css_support',
+	)
+);
diff --git a/src/wp-includes/class-wp-theme-json.php b/src/wp-includes/class-wp-theme-json.php
index c7929dad9e689..b989bab4a6474 100644
--- a/src/wp-includes/class-wp-theme-json.php
+++ b/src/wp-includes/class-wp-theme-json.php
@@ -1520,12 +1520,13 @@ public function get_stylesheet( $types = array( 'variables', 'styles', 'presets'
 	 *
 	 * @since 6.2.0
 	 * @since 6.6.0 Enforced 0-1-0 specificity for block custom CSS selectors.
+	 * @since 7.0.0 Made public for use in custom-css block support.
 	 *
 	 * @param string $css      The CSS to process.
 	 * @param string $selector The selector to nest.
 	 * @return string The processed CSS.
 	 */
-	protected function process_blocks_custom_css( $css, $selector ) {
+	public static function process_blocks_custom_css( $css, $selector ) {
 		$processed_css = '';
 
 		if ( empty( $css ) ) {
diff --git a/src/wp-settings.php b/src/wp-settings.php
index 60c220100f539..a509c37f5e51c 100644
--- a/src/wp-settings.php
+++ b/src/wp-settings.php
@@ -412,6 +412,7 @@
 require ABSPATH . WPINC . '/block-supports/aria-label.php';
 require ABSPATH . WPINC . '/block-supports/anchor.php';
 require ABSPATH . WPINC . '/block-supports/block-visibility.php';
+require ABSPATH . WPINC . '/block-supports/custom-css.php';
 require ABSPATH . WPINC . '/style-engine.php';
 require ABSPATH . WPINC . '/style-engine/class-wp-style-engine.php';
 require ABSPATH . WPINC . '/style-engine/class-wp-style-engine-css-declarations.php';
diff --git a/tests/phpunit/tests/block-supports/wpRenderCustomCssClassName.php b/tests/phpunit/tests/block-supports/wpRenderCustomCssClassName.php
new file mode 100644
index 0000000000000..0bcbc6c708468
--- /dev/null
+++ b/tests/phpunit/tests/block-supports/wpRenderCustomCssClassName.php
@@ -0,0 +1,134 @@
+<?php
+
+/**
+ * @group block-supports
+ *
+ * @covers ::wp_render_custom_css_class_name
+ */
+class Tests_Block_Supports_WpRenderCustomCssClassName extends WP_UnitTestCase {
+
+	/**
+	 * Tests that the custom CSS class name is applied to block content.
+	 *
+	 * @ticket 64544
+	 *
+	 * @covers ::wp_render_custom_css_class_name
+	 *
+	 * @dataProvider data_adds_class_to_content
+	 *
+	 * @param string $block_content  The rendered block content.
+	 * @param array  $block          The block data.
+	 * @param string $expected_class The expected class in the output.
+	 */
+	public function test_adds_class_to_content( $block_content, $block, $expected_class ) {
+		$result = wp_render_custom_css_class_name( $block_content, $block );
+
+		$this->assertStringContainsString( $expected_class, $result, 'Custom CSS class should be present in the output.' );
+	}
+
+	/**
+	 * Data provider.
+	 *
+	 * @return array
+	 */
+	public function data_adds_class_to_content() {
+		return array(
+			'class is added to block content'           => array(
+				'block_content'  => '<div class="wp-block-paragraph">Test content</div>',
+				'block'          => array(
+					'blockName' => 'core/paragraph',
+					'attrs'     => array(
+						'className' => 'wp-custom-css-123abc',
+					),
+				),
+				'expected_class' => 'wp-custom-css-123abc',
+			),
+			'class is extracted from mixed class names' => array(
+				'block_content'  => '<p>Test content</p>',
+				'block'          => array(
+					'blockName' => 'core/paragraph',
+					'attrs'     => array(
+						'className' => 'my-class wp-custom-css-mixed123 another-class',
+					),
+				),
+				'expected_class' => 'wp-custom-css-mixed123',
+			),
+		);
+	}
+
+	/**
+	 * Tests that existing classes are preserved when the custom CSS class is added.
+	 *
+	 * @ticket 64544
+	 *
+	 * @covers ::wp_render_custom_css_class_name
+	 */
+	public function test_preserves_existing_classes() {
+		$block_content = '<div class="existing-class another-class">Test content</div>';
+		$block         = array(
+			'blockName' => 'core/paragraph',
+			'attrs'     => array(
+				'className' => 'wp-custom-css-456def',
+			),
+		);
+
+		$result = wp_render_custom_css_class_name( $block_content, $block );
+
+		$this->assertStringContainsString( 'existing-class', $result, 'Existing classes should be preserved.' );
+		$this->assertStringContainsString( 'another-class', $result, 'All existing classes should be preserved.' );
+		$this->assertStringContainsString( 'wp-custom-css-456def', $result, 'Custom CSS class should be added.' );
+	}
+
+	/**
+	 * Tests that block content is returned unchanged when no custom CSS class should be applied.
+	 *
+	 * @ticket 64544
+	 *
+	 * @covers ::wp_render_custom_css_class_name
+	 *
+	 * @dataProvider data_returns_unchanged_content
+	 *
+	 * @param string $block_content The rendered block content.
+	 * @param array  $block         The block data.
+	 */
+	public function test_returns_unchanged_content( $block_content, $block ) {
+		$result = wp_render_custom_css_class_name( $block_content, $block );
+
+		$this->assertSame( $block_content, $result, 'Block content should remain unchanged.' );
+	}
+
+	/**
+	 * Data provider.
+	 *
+	 * @return array
+	 */
+	public function data_returns_unchanged_content() {
+		return array(
+			'no custom CSS class in attrs'  => array(
+				'block_content' => '<div class="wp-block-paragraph">Test content</div>',
+				'block'         => array(
+					'blockName' => 'core/paragraph',
+					'attrs'     => array(
+						'className' => 'some-other-class',
+					),
+				),
+			),
+			'className is not set in attrs' => array(
+				'block_content' => '<div class="wp-block-paragraph">Test content</div>',
+				'block'         => array(
+					'blockName' => 'core/paragraph',
+					'attrs'     => array(),
+				),
+			),
+			'block content is empty'        => array(
+				'block_content' => '',
+				'block'         => array(
+					'blockName' => 'core/paragraph',
+					'attrs'     => array(
+						'className' => 'wp-custom-css-789ghi',
+					),
+				),
+			),
+		);
+	}
+}
diff --git a/tests/phpunit/tests/block-supports/wpRenderCustomCssSupportStyles.php b/tests/phpunit/tests/block-supports/wpRenderCustomCssSupportStyles.php
new file mode 100644
index 0000000000000..0048b379f8f33
--- /dev/null
+++ b/tests/phpunit/tests/block-supports/wpRenderCustomCssSupportStyles.php
@@ -0,0 +1,267 @@
+<?php
+
+/**
+ * @group block-supports
+ *
+ * @covers ::wp_render_custom_css_support_styles
+ */
+class Tests_Block_Supports_WpRenderCustomCssSupportStyles extends WP_UnitTestCase {
+	/**
+	 * @var string|null
+	 */
+	private $test_block_name;
+
+	public function set_up() {
+		parent::set_up();
+		$this->test_block_name = null;
+	}
+
+	public function tear_down() {
+		if ( $this->test_block_name ) {
+			unregister_block_type( $this->test_block_name );
+		}
+		$this->test_block_name = null;
+		parent::tear_down();
+	}
+
+	/**
+	 * Tests that custom CSS support adds a class name when valid CSS is present.
+	 *
+	 * @ticket 64544
+	 *
+	 * @covers ::wp_render_custom_css_support_styles
+	 *
+	 * @dataProvider data_adds_class_name
+	 *
+	 * @param string $block_name   The test block name to register.
+	 * @param array  $supports     The block support configuration.
+	 * @param array  $parsed_block The parsed block data.
+	 */
+	public function test_adds_class_name( $block_name, $supports, $parsed_block ) {
+		$this->test_block_name = $block_name;
+		register_block_type(
+			$this->test_block_name,
+			array(
+				'api_version' => 3,
+				'attributes'  => array(
+					'style' => array(
+						'type' => 'object',
+					),
+				),
+				'supports'    => $supports,
+			)
+		);
+
+		$result = wp_render_custom_css_support_styles( $parsed_block );
+
+		$this->assertArrayHasKey( 'className', $result['attrs'], 'Block should have className added.' );
+		$this->assertMatchesRegularExpression( '/wp-custom-css-/', $result['attrs']['className'], 'className should contain wp-custom-css- prefix.' );
+	}
+
+	/**
+	 * Data provider.
+	 *
+	 * @return array
+	 */
+	public function data_adds_class_name() {
+		return array(
+			'class name is added when custom CSS is present'         => array(
+				'block_name'   => 'test/custom-css-block',
+				'supports'     => array( 'customCSS' => true ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-block',
+					'attrs'     => array(
+						'style' => array(
+							'css' => 'color: red;',
+						),
+					),
+				),
+			),
+			'class name is added when support is not explicitly set' => array(
+				'block_name'   => 'test/custom-css-default',
+				'supports'     => array(),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-default',
+					'attrs'     => array(
+						'style' => array(
+							'css' => 'font-weight: bold;',
+						),
+					),
+				),
+			),
+			'class name is added for valid CSS with url() values'    => array(
+				'block_name'   => 'test/custom-css-valid',
+				'supports'     => array( 'customCSS' => true ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-valid',
+					'attrs'     => array(
+						'style' => array(
+							'css' => 'color: red; background: url("image.png"); font-size: 16px;',
+						),
+					),
+				),
+			),
+		);
+	}
+
+	/**
+	 * Tests that existing className is preserved when custom CSS class is added.
+	 *
+	 * @ticket 64544
+	 *
+	 * @covers ::wp_render_custom_css_support_styles
+	 */
+	public function test_preserves_existing_class_name() {
+		$this->test_block_name = 'test/custom-css-block-existing';
+		register_block_type(
+			$this->test_block_name,
+			array(
+				'api_version' => 3,
+				'attributes'  => array(
+					'style' => array(
+						'type' => 'object',
+					),
+				),
+				'supports'    => array( 'customCSS' => true ),
+			)
+		);
+
+		$parsed_block = array(
+			'blockName' => 'test/custom-css-block-existing',
+			'attrs'     => array(
+				'className' => 'my-existing-class',
+				'style'     => array(
+					'css' => 'color: blue;',
+				),
+			),
+		);
+
+		$result = wp_render_custom_css_support_styles( $parsed_block );
+
+		$this->assertStringContainsString( 'my-existing-class', $result['attrs']['className'], 'Existing className should be preserved.' );
+		$this->assertMatchesRegularExpression( '/wp-custom-css-/', $result['attrs']['className'], 'className should also contain wp-custom-css- prefix.' );
+	}
+
+	/**
+	 * Tests that custom CSS support does not add a class name when CSS should not be applied.
+	 *
+	 * @ticket 64544
+	 *
+	 * @covers ::wp_render_custom_css_support_styles
+	 *
+	 * @dataProvider data_does_not_add_class_name
+	 *
+	 * @param string $block_name   The test block name to register.
+	 * @param array  $supports     The block support configuration.
+	 * @param array  $parsed_block The parsed block data.
+	 */
+	public function test_does_not_add_class_name( $block_name, $supports, $parsed_block ) {
+		$this->test_block_name = $block_name;
+		register_block_type(
+			$this->test_block_name,
+			array(
+				'api_version' => 3,
+				'attributes'  => array(
+					'style' => array(
+						'type' => 'object',
+					),
+				),
+				'supports'    => $supports,
+			)
+		);
+
+		$result = wp_render_custom_css_support_styles( $parsed_block );
+
+		$this->assertArrayNotHasKey( 'className', $result['attrs'], 'Block should not have className added.' );
+	}
+
+	/**
+	 * Data provider.
+	 *
+	 * @return array
+	 */
+	public function data_does_not_add_class_name() {
+		return array(
+			'support is disabled'            => array(
+				'block_name'   => 'test/custom-css-disabled',
+				'supports'     => array( 'customCSS' => false ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-disabled',
+					'attrs'     => array(
+						'style' => array(
+							'css' => 'color: green;',
+						),
+					),
+				),
+			),
+			'no CSS attribute present'       => array(
+				'block_name'   => 'test/custom-css-no-css',
+				'supports'     => array( 'customCSS' => true ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-no-css',
+					'attrs'     => array(
+						'style' => array(
+							'color' => 'red',
+						),
+					),
+				),
+			),
+			'CSS is empty'                   => array(
+				'block_name'   => 'test/custom-css-empty',
+				'supports'     => array( 'customCSS' => true ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-empty',
+					'attrs'     => array(
+						'style' => array(
+							'css' => '',
+						),
+					),
+				),
+			),
+			'CSS is whitespace only'         => array(
+				'block_name'   => 'test/custom-css-whitespace',
+				'supports'     => array( 'customCSS' => true ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-whitespace',
+					'attrs'     => array(
+						'style' => array(
+							'css' => '   ',
+						),
+					),
+				),
+			),
+			'no style attribute'             => array(
+				'block_name'   => 'test/custom-css-no-style',
+				'supports'     => array( 'customCSS' => true ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-no-style',
+					'attrs'     => array(),
+				),
+			),
+			'CSS contains HTML opening tags' => array(
+				'block_name'   => 'test/custom-css-html-open',
+				'supports'     => array( 'customCSS' => true ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-html-open',
+					'attrs'     => array(
+						'style' => array(
+							'css' => '<script>alert(1)</script>',
+						),
+					),
+				),
+			),
+			'CSS contains HTML closing tags' => array(
+				'block_name'   => 'test/custom-css-html-close',
+				'supports'     => array( 'customCSS' => true ),
+				'parsed_block' => array(
+					'blockName' => 'test/custom-css-html-close',
+					'attrs'     => array(
+						'style' => array(
+							'css' => 'color: red;</style><script>alert(1)</script>',
+						),
+					),
+				),
+			),
+		);
+	}
+}
diff --git a/tests/phpunit/tests/blocks/editor.php b/tests/phpunit/tests/blocks/editor.php
index 4241161388eb8..1de4dbf1719a6 100644
--- a/tests/phpunit/tests/blocks/editor.php
+++ b/tests/phpunit/tests/blocks/editor.php
@@ -583,7 +583,8 @@ public function test_get_block_editor_settings_deprecated_filter_post_editor() {
 
 		$this->assertSameSets(
 			array(
-				'filter' => 'deprecated',
+				'canEditCSS' => false,
+				'filter'     => 'deprecated',
 			),
 			$settings
 		);