diff --git a/src/js/_enqueues/wp/customize/preview.js b/src/js/_enqueues/wp/customize/preview.js
index bcff0bc25166c..2055b5e792ee5 100644
--- a/src/js/_enqueues/wp/customize/preview.js
+++ b/src/js/_enqueues/wp/customize/preview.js
@@ -635,11 +635,22 @@
 		/**
 		 * Preview changes to custom css.
 		 *
-		 * @param {string} value Custom CSS..
+		 * @param {string} value Custom CSS.
 		 * @return {void}
 		 */
 		custom_css: function( value ) {
-			$( '#wp-custom-css' ).text( value );
+			var style;
+			if ( api.settings.theme.isBlockTheme ) {
+				style = $( 'style#global-styles-inline-css' );
+				value = value.replace( /\/\*(BEGIN|END)_CUSTOMIZER_CUSTOM_CSS\*\//g, '' ); // Forbid milestone comments from appearing in Custom CSS which would break live preview.
+				var textContent = style.text().replace( /(\/\*BEGIN_CUSTOMIZER_CUSTOM_CSS\*\/)((?:.|\s)*?)(\/\*END_CUSTOMIZER_CUSTOM_CSS\*\/)/, function ( match, beforeComment, oldValue, afterComment ) {
+					return beforeComment + '\n' + value + '\n' + afterComment;
+				} );
+				style.text( textContent );
+			} else {
+				style = $( 'style#wp-custom-css' );
+				style.text( value );
+			}
 		},
 
 		/**
diff --git a/src/wp-includes/class-wp-customize-manager.php b/src/wp-includes/class-wp-customize-manager.php
index 0d41d4a09bdcb..6a656808ae5a1 100644
--- a/src/wp-includes/class-wp-customize-manager.php
+++ b/src/wp-includes/class-wp-customize-manager.php
@@ -2161,8 +2161,9 @@ public function customize_preview_settings() {
 				'keepAliveSend'    => 1000,
 			),
 			'theme'             => array(
-				'stylesheet' => $this->get_stylesheet(),
-				'active'     => $this->is_theme_active(),
+				'stylesheet'   => $this->get_stylesheet(),
+				'active'       => $this->is_theme_active(),
+				'isBlockTheme' => wp_is_block_theme(),
 			),
 			'url'               => array(
 				'self'          => $self_url,
diff --git a/src/wp-includes/script-loader.php b/src/wp-includes/script-loader.php
index 3beddac135e43..54193c841c7c3 100644
--- a/src/wp-includes/script-loader.php
+++ b/src/wp-includes/script-loader.php
@@ -2541,8 +2541,27 @@ function wp_enqueue_global_styles() {
 		 * and add it before the global styles custom CSS.
 		 */
 		remove_action( 'wp_head', 'wp_custom_css_cb', 101 );
-		// Get the custom CSS from the Customizer and add it to the global stylesheet.
-		$custom_css  = wp_get_custom_css();
+
+		/*
+		 * Get the custom CSS from the Customizer and add it to the global stylesheet.
+		 * Always do this in Customizer preview for the sake of live preview since it be empty.
+		 */
+		$custom_css = trim( wp_get_custom_css() );
+		if ( $custom_css || is_customize_preview() ) {
+			if ( is_customize_preview() ) {
+				/*
+				 * When in the Customizer preview, wrap the Custom CSS in milestone comments to allow customize-preview.js
+				 * to locate the CSS to replace for live previewing. Make sure that the milestone comments are omitted from
+				 * the stored Custom CSS if by chance someone tried to add them, which would be highly unlikely, but it
+				 * would break live previewing.
+				 */
+				$before_milestone = '/*BEGIN_CUSTOMIZER_CUSTOM_CSS*/';
+				$after_milestone  = '/*END_CUSTOMIZER_CUSTOM_CSS*/';
+				$custom_css       = str_replace( array( $before_milestone, $after_milestone ), '', $custom_css );
+				$custom_css       = $before_milestone . "\n" . $custom_css . "\n" . $after_milestone;
+			}
+			$custom_css = "\n" . $custom_css;
+		}
 		$stylesheet .= $custom_css;
 
 		// Add the global styles custom CSS at the end.