diff --git a/src/wp-includes/block-editor.php b/src/wp-includes/block-editor.php
index 4227c674c02ff..72a91ce061db5 100644
--- a/src/wp-includes/block-editor.php
+++ b/src/wp-includes/block-editor.php
@@ -428,6 +428,12 @@ 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 separate style sheet so any invalid CSS entered by users does not break other global styles.
+		$editor_settings['styles'][] = array(
+			'css'            => wp_get_global_stylesheet( array( '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 f9e8e371c596a..6e4b12ed64ec7 100644
--- a/src/wp-includes/class-wp-theme-json.php
+++ b/src/wp-includes/class-wp-theme-json.php
@@ -403,6 +403,7 @@ class WP_Theme_JSON {
 			'textDecoration' => null,
 			'textTransform'  => null,
 		),
+		'css'        => null,
 	);
 
 	/**
@@ -952,6 +953,11 @@ public function get_stylesheet( $types = array( 'variables', 'styles', 'presets'
 			$stylesheet .= $this->get_preset_classes( $setting_nodes, $origins );
 		}
 
+		// Load the custom CSS last so it has the highest specificity.
+		if ( in_array( 'custom-css', $types, true ) ) {
+			$stylesheet .= _wp_array_get( $this->theme_json, array( 'styles', 'css' ) );
+		}
+
 		return $stylesheet;
 	}
 
diff --git a/src/wp-includes/global-styles-and-settings.php b/src/wp-includes/global-styles-and-settings.php
index c625166524b63..fca29dd4ca021 100644
--- a/src/wp-includes/global-styles-and-settings.php
+++ b/src/wp-includes/global-styles-and-settings.php
@@ -75,6 +75,7 @@ function wp_get_global_styles( $path = array(), $context = array() ) {
  * Returns the stylesheet resulting of merging core, theme, and user data.
  *
  * @since 5.9.0
+ * @since 6.2.0 Support for custom-css type added.
  *
  * @param array $types Types of styles to load. Optional.
  *                     It accepts 'variables', 'styles', 'presets' as values.
@@ -106,7 +107,7 @@ function wp_get_global_stylesheet( $types = array() ) {
 	if ( empty( $types ) && ! $supports_theme_json ) {
 		$types = array( 'variables', 'presets', 'base-layout-styles' );
 	} elseif ( empty( $types ) ) {
-		$types = array( 'variables', 'styles', 'presets' );
+		$types = array( 'variables', 'styles', 'presets', 'custom-css' );
 	}
 
 	/*
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 9ce931398f383..3a476b02ff441 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;
@@ -290,6 +294,7 @@ 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.
@@ -313,6 +318,10 @@ protected function prepare_item_for_database( $request ) {
 			$config = array();
 			if ( isset( $request['styles'] ) ) {
 				$config['styles'] = $request['styles'];
+				$validate_custom_css = $this->validate_custom_css( $request['styles']['css'] );
+				if ( is_wp_error( $validate_custom_css ) ) {
+					return $validate_custom_css;
+				}
 			} elseif ( isset( $existing_config['styles'] ) ) {
 				$config['styles'] = $existing_config['styles'];
 			}
@@ -652,4 +661,25 @@ 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.', 'gutenberg' ),
+				array( 'status' => 400 )
+			);
+		}
+		return true;
+	}
 }