diff --git a/lib/class-wp-theme-json-gutenberg.php b/lib/class-wp-theme-json-gutenberg.php
index 97b9c58b13df29..b23bb678fb725b 100644
--- a/lib/class-wp-theme-json-gutenberg.php
+++ b/lib/class-wp-theme-json-gutenberg.php
@@ -1138,9 +1138,27 @@ protected function process_blocks_custom_css( $css, $selector ) {
 		// Split CSS nested rules.
 		$parts = explode( '&', $css );
 		foreach ( $parts as $part ) {
-			$processed_css .= ( ! str_contains( $part, '{' ) )
-				? trim( $selector ) . '{' . trim( $part ) . '}' // If the part doesn't contain braces, it applies to the root level.
-				: trim( $selector . $part ); // Prepend the selector, which effectively replaces the "&" character.
+			$is_root_css = ( ! str_contains( $part, '{' ) );
+			if ( $is_root_css ) {
+				// If the part doesn't contain braces, it applies to the root level.
+				$processed_css .= trim( $selector ) . '{' . trim( $part ) . '}';
+			} else {
+				// If the part contains braces, it's a nested CSS rule.
+				$part = explode( '{', str_replace( '}', '', $part ) );
+				if ( count( $part ) !== 2 ) {
+					continue;
+				}
+				$nested_selector    = $part[0];
+				$css_value          = $part[1];
+				$root_selectors     = explode( ',', $selector );
+				$combined_selectors = array_map(
+					static function( $root_selector ) use ( $nested_selector ) {
+						return $root_selector . $nested_selector;
+					},
+					$root_selectors
+				);
+				$processed_css     .= implode( ',', $combined_selectors ) . '{' . trim( $css_value ) . '}';
+			}
 		}
 		return $processed_css;
 	}
diff --git a/packages/block-editor/src/components/global-styles/use-global-styles-output.js b/packages/block-editor/src/components/global-styles/use-global-styles-output.js
index 1db7e46c6eb775..492b55f6262ba3 100644
--- a/packages/block-editor/src/components/global-styles/use-global-styles-output.js
+++ b/packages/block-editor/src/components/global-styles/use-global-styles-output.js
@@ -1127,9 +1127,26 @@ const processCSSNesting = ( css, blockSelector ) => {
 	// Split CSS nested rules.
 	const parts = css.split( '&' );
 	parts.forEach( ( part ) => {
-		processedCSS += ! part.includes( '{' )
-			? blockSelector + '{' + part + '}' // If the part doesn't contain braces, it applies to the root level.
-			: blockSelector + part; // Prepend the selector, which effectively replaces the "&" character.
+		const isRootCss = ! part.includes( '{' );
+		if ( isRootCss ) {
+			// If the part doesn't contain braces, it applies to the root level.
+			processedCSS += `${ blockSelector }{${ part }}`;
+		} else {
+			// If the part contains braces, it's a nested CSS rule.
+			const splittedPart = part.replace( '}', '' ).split( '{' );
+			if ( splittedPart.length !== 2 ) {
+				return;
+			}
+
+			const [ nestedSelector, cssValue ] = splittedPart;
+			const rootSelectors = blockSelector.split( ',' );
+			const combinedSelectors = rootSelectors.map(
+				( rootSelector ) => rootSelector + nestedSelector
+			);
+			processedCSS += `${ combinedSelectors.join(
+				', '
+			) }{${ cssValue.trim() }}`;
+		}
 	} );
 	return processedCSS;
 };
diff --git a/phpunit/class-wp-theme-json-test.php b/phpunit/class-wp-theme-json-test.php
index 11ec35e0925bfe..c5881b100538d5 100644
--- a/phpunit/class-wp-theme-json-test.php
+++ b/phpunit/class-wp-theme-json-test.php
@@ -2033,6 +2033,14 @@ public function data_process_blocks_custom_css() {
 				),
 				'expected' => '.foo{color: red; margin: auto;}.foo .bar{color: blue;}.foo::before{color: green;}',
 			),
+			// CSS with multiple root selectors.
+			'with multiple root selectors'      => array(
+				'input'    => array(
+					'selector' => '.foo, .bar',
+					'css'      => 'color: red; margin: auto; & .baz{color: blue;} &::before{color: green;}',
+				),
+				'expected' => '.foo, .bar{color: red; margin: auto;}.foo .baz, .bar .baz{color: blue;}.foo::before, .bar::before{color: green;}',
+			),
 		);
 	}