diff --git a/src/wp-includes/block-editor.php b/src/wp-includes/block-editor.php
index bbb139d756c1a..acf7b5d55089b 100644
--- a/src/wp-includes/block-editor.php
+++ b/src/wp-includes/block-editor.php
@@ -410,6 +410,16 @@ function get_block_editor_settings( array $custom_settings, $block_editor_contex
 			$block_classes['css'] = $actual_css;
 			$global_styles[]      = $block_classes;
 		}
+
+		/*
+		 * Add the custom CSS as a separate stylesheet so any invalid CSS
+		 * entered by users does not break other global styles.
+		 */
+		$editor_settings['styles'][] = array(
+			'css'            => wp_get_global_styles_custom_css(),
+			'__unstableType' => 'user',
+			'isGlobalStyles' => true,
+		);
 	} else {
 		// If there is no `theme.json` file, ensure base layout styles are still available.
 		$block_classes = array(
diff --git a/src/wp-includes/class-wp-theme-json.php b/src/wp-includes/class-wp-theme-json.php
index 71801df2af174..2908fb94d7e69 100644
--- a/src/wp-includes/class-wp-theme-json.php
+++ b/src/wp-includes/class-wp-theme-json.php
@@ -425,6 +425,7 @@ class WP_Theme_JSON {
 			'textDecoration' => null,
 			'textTransform'  => null,
 		),
+		'css'        => null,
 	);
 
 	/**
@@ -1005,6 +1006,31 @@ public function get_stylesheet( $types = array( 'variables', 'styles', 'presets'
 		return $stylesheet;
 	}
 
+	/**
+	 * Returns the global styles custom css.
+	 *
+	 * @since 6.2.0
+	 *
+	 * @return string
+	 */
+	public function get_custom_css() {
+		// Add the global styles root CSS.
+		$stylesheet = _wp_array_get( $this->theme_json, array( 'styles', 'css' ), '' );
+
+		// Add the global styles block CSS.
+		if ( isset( $this->theme_json['styles']['blocks'] ) ) {
+			foreach ( $this->theme_json['styles']['blocks'] as $name => $node ) {
+				$custom_block_css = _wp_array_get( $this->theme_json, array( 'styles', 'blocks', $name, 'css' ) );
+				if ( $custom_block_css ) {
+					$selector    = static::$blocks_metadata[ $name ]['selector'];
+					$stylesheet .= $this->process_blocks_custom_css( $custom_block_css, $selector );
+				}
+			}
+		}
+
+		return $stylesheet;
+	}
+
 	/**
 	 * Returns the page templates of the active theme.
 	 *
@@ -2740,7 +2766,12 @@ public static function remove_insecure_properties( $theme_json ) {
 				continue;
 			}
 
-			$output = static::remove_insecure_styles( $input );
+			// The global styles custom CSS is not sanitized, but can only be edited by users with 'edit_css' capability.
+			if ( isset( $input['css'] ) && current_user_can( 'edit_css' ) ) {
+				$output = $input;
+			} else {
+				$output = static::remove_insecure_styles( $input );
+			}
 
 			/*
 			 * Get a reference to element name from path.
diff --git a/src/wp-includes/default-filters.php b/src/wp-includes/default-filters.php
index 4e6340700cc15..09be9e576b6d2 100644
--- a/src/wp-includes/default-filters.php
+++ b/src/wp-includes/default-filters.php
@@ -577,6 +577,9 @@
 add_action( 'wp_enqueue_scripts', 'wp_enqueue_global_styles' );
 add_action( 'wp_footer', 'wp_enqueue_global_styles', 1 );
 
+// Global styles custom CSS.
+add_action( 'wp_enqueue_scripts', 'wp_enqueue_global_styles_custom_css' );
+
 // Block supports, and other styles parsed and stored in the Style Engine.
 add_action( 'wp_enqueue_scripts', 'wp_enqueue_stored_styles' );
 add_action( 'wp_footer', 'wp_enqueue_stored_styles', 1 );
diff --git a/src/wp-includes/global-styles-and-settings.php b/src/wp-includes/global-styles-and-settings.php
index 8195aaaa34b2a..fe2393abea974 100644
--- a/src/wp-includes/global-styles-and-settings.php
+++ b/src/wp-includes/global-styles-and-settings.php
@@ -225,6 +225,60 @@ function wp_get_global_stylesheet( $types = array() ) {
 	return $stylesheet;
 }
 
+/**
+ * Gets the global styles custom css from theme.json.
+ *
+ * @since 6.2.0
+ *
+ * @return string Stylesheet.
+ */
+function wp_get_global_styles_custom_css() {
+	if ( ! wp_theme_has_theme_json() ) {
+		return '';
+	}
+	/*
+	 * Ignore cache when `WP_DEBUG` is enabled, so it doesn't interfere with the theme
+	 * developer's workflow.
+	 *
+	 * @todo Replace `WP_DEBUG` once an "in development mode" check is available in Core.
+	 */
+	$can_use_cached = ! WP_DEBUG;
+
+	/*
+	 * By using the 'theme_json' group, this data is marked to be non-persistent across requests.
+	 * @see `wp_cache_add_non_persistent_groups()`.
+	 *
+	 * The rationale for this is to make sure derived data from theme.json
+	 * is always fresh from the potential modifications done via hooks
+	 * that can use dynamic data (modify the stylesheet depending on some option,
+	 * settings depending on user permissions, etc.).
+	 * See some of the existing hooks to modify theme.json behavior:
+	 * @see https://make.wordpress.org/core/2022/10/10/filters-for-theme-json-data/
+	 *
+	 * A different alternative considered was to invalidate the cache upon certain
+	 * events such as options add/update/delete, user meta, etc.
+	 * It was judged not enough, hence this approach.
+	 * @see https://github.com/WordPress/gutenberg/pull/45372
+	 */
+	$cache_key   = 'wp_get_global_styles_custom_css';
+	$cache_group = 'theme_json';
+	if ( $can_use_cached ) {
+		$cached = wp_cache_get( $cache_key, $cache_group );
+		if ( $cached ) {
+			return $cached;
+		}
+	}
+
+	$tree       = WP_Theme_JSON_Resolver::get_merged_data();
+	$stylesheet = $tree->get_custom_css();
+
+	if ( $can_use_cached ) {
+		wp_cache_set( $cache_key, $stylesheet, $cache_group );
+	}
+
+	return $stylesheet;
+}
+
 /**
  * Returns a string containing the SVGs to be referenced as filters (duotone).
  *
@@ -369,5 +423,6 @@ function wp_clean_theme_json_cache() {
 	wp_cache_delete( 'wp_get_global_styles_svg_filters', 'theme_json' );
 	wp_cache_delete( 'wp_get_global_settings_custom', 'theme_json' );
 	wp_cache_delete( 'wp_get_global_settings_theme', 'theme_json' );
+	wp_cache_delete( 'wp_get_global_styles_custom_css', 'theme_json' );
 	WP_Theme_JSON_Resolver::clean_cached_data();
 }
diff --git a/src/wp-includes/rest-api/endpoints/class-wp-rest-global-styles-controller.php b/src/wp-includes/rest-api/endpoints/class-wp-rest-global-styles-controller.php
index b504e23c35ba6..c8eee60ed3632 100644
--- a/src/wp-includes/rest-api/endpoints/class-wp-rest-global-styles-controller.php
+++ b/src/wp-includes/rest-api/endpoints/class-wp-rest-global-styles-controller.php
@@ -268,6 +268,10 @@ public function update_item( $request ) {
 		}
 
 		$changes = $this->prepare_item_for_database( $request );
+		if ( is_wp_error( $changes ) ) {
+			return $changes;
+		}
+
 		$result  = wp_update_post( wp_slash( (array) $changes ), true, false );
 		if ( is_wp_error( $result ) ) {
 			return $result;
@@ -290,9 +294,10 @@ public function update_item( $request ) {
 	 * Prepares a single global styles config for update.
 	 *
 	 * @since 5.9.0
+	 * @since 6.2.0 Added validation of styles.css property.
 	 *
 	 * @param WP_REST_Request $request Request object.
-	 * @return stdClass Changes to pass to wp_update_post.
+	 * @return stdClass|WP_Error Prepared item on success. WP_Error on when the custom CSS is not valid.
 	 */
 	protected function prepare_item_for_database( $request ) {
 		$changes     = new stdClass();
@@ -312,6 +317,12 @@ protected function prepare_item_for_database( $request ) {
 		if ( isset( $request['styles'] ) || isset( $request['settings'] ) ) {
 			$config = array();
 			if ( isset( $request['styles'] ) ) {
+				if ( isset( $request['styles']['css'] ) ) {
+					$css_validation_result = $this->validate_custom_css( $request['styles']['css'] );
+					if ( is_wp_error( $css_validation_result ) ) {
+						return $css_validation_result;
+					}
+				}
 				$config['styles'] = $request['styles'];
 			} elseif ( isset( $existing_config['styles'] ) ) {
 				$config['styles'] = $existing_config['styles'];
@@ -657,4 +668,25 @@ public function get_theme_items( $request ) {
 
 		return $response;
 	}
+
+	/**
+	 * Validate style.css as valid CSS.
+	 *
+	 * Currently just checks for invalid markup.
+	 *
+	 * @since 6.2.0
+	 *
+	 * @param string $css CSS to validate.
+	 * @return true|WP_Error True if the input was validated, otherwise WP_Error.
+	 */
+	private function validate_custom_css( $css ) {
+		if ( preg_match( '#</?\w+#', $css ) ) {
+			return new WP_Error(
+				'rest_custom_css_illegal_markup',
+				__( 'Markup is not allowed in CSS.' ),
+				array( 'status' => 400 )
+			);
+		}
+		return true;
+	}
 }
diff --git a/src/wp-includes/script-loader.php b/src/wp-includes/script-loader.php
index 63f5c4fe28f39..2245b08c5717d 100644
--- a/src/wp-includes/script-loader.php
+++ b/src/wp-includes/script-loader.php
@@ -2454,6 +2454,27 @@ function wp_enqueue_global_styles() {
 	wp_add_global_styles_for_blocks();
 }
 
+/**
+ * Enqueues the global styles custom css defined via theme.json.
+ *
+ * @since 6.2.0
+ */
+function wp_enqueue_global_styles_custom_css() {
+	if ( ! wp_is_block_theme() ) {
+		return;
+	}
+
+	// Don't enqueue Customizer's custom CSS separately.
+	remove_action( 'wp_head', 'wp_custom_css_cb', 101 );
+
+	$custom_css  = wp_get_custom_css();
+	$custom_css .= wp_get_global_styles_custom_css();
+
+	if ( ! empty( $custom_css ) ) {
+		wp_add_inline_style( 'global-styles', $custom_css );
+	}
+}
+
 /**
  * Renders the SVG filters supplied by theme.json.
  *
diff --git a/tests/phpunit/tests/rest-api/rest-global-styles-controller.php b/tests/phpunit/tests/rest-api/rest-global-styles-controller.php
index 8fc86d2205c7f..f20fde92ae663 100644
--- a/tests/phpunit/tests/rest-api/rest-global-styles-controller.php
+++ b/tests/phpunit/tests/rest-api/rest-global-styles-controller.php
@@ -532,4 +532,43 @@ public function test_assign_edit_css_action_admin() {
 			$this->assertArrayHasKey( 'https://api.w.org/action-edit-css', $links );
 		}
 	}
+
+	/**
+	 * @covers WP_REST_Global_Styles_Controller::update_item
+	 * @ticket 57536
+	 */
+	public function test_update_item_valid_styles_css() {
+		wp_set_current_user( self::$admin_id );
+		if ( is_multisite() ) {
+			grant_super_admin( self::$admin_id );
+		}
+		$request = new WP_REST_Request( 'PUT', '/wp/v2/global-styles/' . self::$global_styles_id );
+		$request->set_body_params(
+			array(
+				'styles' => array( 'css' => 'body { color: red; }' ),
+			)
+		);
+		$response = rest_get_server()->dispatch( $request );
+		$data     = $response->get_data();
+		$this->assertSame( 'body { color: red; }', $data['styles']['css'] );
+	}
+
+	/**
+	 * @covers WP_REST_Global_Styles_Controller::update_item
+	 * @ticket 57536
+	 */
+	public function test_update_item_invalid_styles_css() {
+		wp_set_current_user( self::$admin_id );
+		if ( is_multisite() ) {
+			grant_super_admin( self::$admin_id );
+		}
+		$request = new WP_REST_Request( 'PUT', '/wp/v2/global-styles/' . self::$global_styles_id );
+		$request->set_body_params(
+			array(
+				'styles' => array( 'css' => '<p>test</p> body { color: red; }' ),
+			)
+		);
+		$response = rest_get_server()->dispatch( $request );
+		$this->assertErrorResponse( 'rest_custom_css_illegal_markup', $response, 400 );
+	}
 }
diff --git a/tests/phpunit/tests/theme/wpThemeJson.php b/tests/phpunit/tests/theme/wpThemeJson.php
index 113a1f01800ab..efa709ef756dc 100644
--- a/tests/phpunit/tests/theme/wpThemeJson.php
+++ b/tests/phpunit/tests/theme/wpThemeJson.php
@@ -14,6 +14,36 @@
  */
 class Tests_Theme_wpThemeJson extends WP_UnitTestCase {
 
+	/**
+	 * Administrator ID.
+	 *
+	 * @var int
+	 */
+	private static $administrator_id;
+
+	/**
+	 * User ID.
+	 *
+	 * @var int
+	 */
+	private static $user_id;
+
+	public static function set_up_before_class() {
+		parent::set_up_before_class();
+
+		static::$administrator_id = self::factory()->user->create(
+			array(
+				'role' => 'administrator',
+			)
+		);
+
+		if ( is_multisite() ) {
+			grant_super_admin( self::$administrator_id );
+		}
+
+		static::$user_id = self::factory()->user->create();
+	}
+
 	/**
 	 * @ticket 52991
 	 * @ticket 54336
@@ -4505,4 +4535,93 @@ public function test_get_shadow_styles_for_blocks() {
 
 		$this->assertSame( $expected_styles, $theme_json->get_stylesheet() );
 	}
+
+	/**
+	 * @ticket 57536
+	 */
+	public function test_get_custom_css_handles_global_custom_css() {
+		$theme_json = new WP_Theme_JSON(
+			array(
+				'version' => WP_Theme_JSON::LATEST_SCHEMA,
+				'styles'  => array(
+					'css' => 'body { color:purple; }',
+				),
+			)
+		);
+		$custom_css = 'body { color:purple; }';
+		$this->assertSame( $custom_css, $theme_json->get_custom_css() );
+	}
+
+	/**
+	 * Tests that custom CSS is kept for users with correct capabilities and removed for others.
+	 *
+	 * @ticket 57536
+	 *
+	 * @dataProvider data_custom_css_for_user_caps
+	 *
+	 * @param string $user_property The property name for current user.
+	 * @param array  $expected      Expected results.
+	 */
+	public function test_custom_css_for_user_caps( $user_property, array $expected ) {
+		wp_set_current_user( static::${$user_property} );
+
+		$actual = WP_Theme_JSON::remove_insecure_properties(
+			array(
+				'version' => WP_Theme_JSON::LATEST_SCHEMA,
+				'styles'  => array(
+					'css'    => 'body { color:purple; }',
+					'blocks' => array(
+						'core/separator' => array(
+							'color' => array(
+								'background' => 'blue',
+							),
+						),
+					),
+				),
+			)
+		);
+
+		$this->assertSameSetsWithIndex( $expected, $actual );
+	}
+
+	/**
+	 * Data provider.
+	 *
+	 * @return array[]
+	 */
+	public function data_custom_css_for_user_caps() {
+		return array(
+			'allows custom css for users with caps'     => array(
+				'user_property' => 'administrator_id',
+				'expected'      => array(
+					'version' => WP_Theme_JSON::LATEST_SCHEMA,
+					'styles'  => array(
+						'css'    => 'body { color:purple; }',
+						'blocks' => array(
+							'core/separator' => array(
+								'color' => array(
+									'background' => 'blue',
+								),
+							),
+						),
+					),
+				),
+			),
+			'removes custom css for users without caps' => array(
+				'user_property' => 'user_id',
+				'expected'      => array(
+					'version' => WP_Theme_JSON::LATEST_SCHEMA,
+					'styles'  => array(
+						'blocks' => array(
+							'core/separator' => array(
+								'color' => array(
+									'background' => 'blue',
+								),
+							),
+						),
+					),
+				),
+			),
+		);
+	}
 }