diff --git a/lib/class-wp-theme-json-gutenberg.php b/lib/class-wp-theme-json-gutenberg.php
index 59a3bbc3eb2ef6..3aa07158df8534 100644
--- a/lib/class-wp-theme-json-gutenberg.php
+++ b/lib/class-wp-theme-json-gutenberg.php
@@ -1145,9 +1145,23 @@ 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];
+				$part_selector   = str_starts_with( $nested_selector, ' ' )
+					? static::scope_selector( $selector, $nested_selector )
+					: static::append_to_selector( $selector, $nested_selector );
+				$processed_css  .= $part_selector . '{' . trim( $css_value ) . '}';
+			}
 		}
 		return $processed_css;
 	}
diff --git a/packages/block-editor/src/components/global-styles/test/use-global-styles-output.js b/packages/block-editor/src/components/global-styles/test/use-global-styles-output.js
index 1aead846e95cdb..b05381a8325b06 100644
--- a/packages/block-editor/src/components/global-styles/test/use-global-styles-output.js
+++ b/packages/block-editor/src/components/global-styles/test/use-global-styles-output.js
@@ -14,6 +14,7 @@ import {
 	toCustomProperties,
 	toStyles,
 	getStylesDeclarations,
+	processCSSNesting,
 } from '../use-global-styles-output';
 import { ROOT_BLOCK_SELECTOR } from '../utils';
 
@@ -967,4 +968,42 @@ describe( 'global styles renderer', () => {
 			] );
 		} );
 	} );
+
+	describe( 'processCSSNesting', () => {
+		it( 'should return processed CSS without any nested selectors', () => {
+			expect(
+				processCSSNesting( 'color: red; margin: auto;', '.foo' )
+			).toEqual( '.foo{color: red; margin: auto;}' );
+		} );
+		it( 'should return processed CSS with nested selectors', () => {
+			expect(
+				processCSSNesting(
+					'color: red; margin: auto; &.one{color: blue;} & .two{color: green;}',
+					'.foo'
+				)
+			).toEqual(
+				'.foo{color: red; margin: auto;}.foo.one{color: blue;}.foo .two{color: green;}'
+			);
+		} );
+		it( 'should return processed CSS with pseudo elements', () => {
+			expect(
+				processCSSNesting(
+					'color: red; margin: auto; &::before{color: blue;} & ::before{color: green;}  &.one::before{color: yellow;} & .two::before{color: purple;}',
+					'.foo'
+				)
+			).toEqual(
+				'.foo{color: red; margin: auto;}.foo::before{color: blue;}.foo ::before{color: green;}.foo.one::before{color: yellow;}.foo .two::before{color: purple;}'
+			);
+		} );
+		it( 'should return processed CSS with multiple root selectors', () => {
+			expect(
+				processCSSNesting(
+					'color: red; margin: auto; &.one{color: blue;} & .two{color: green;} &::before{color: yellow;} & ::before{color: purple;}  &.three::before{color: orange;} & .four::before{color: skyblue;}',
+					'.foo, .bar'
+				)
+			).toEqual(
+				'.foo, .bar{color: red; margin: auto;}.foo.one, .bar.one{color: blue;}.foo .two, .bar .two{color: green;}.foo::before, .bar::before{color: yellow;}.foo ::before, .bar ::before{color: purple;}.foo.three::before, .bar.three::before{color: orange;}.foo .four::before, .bar .four::before{color: skyblue;}'
+			);
+		} );
+	} );
 } );
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 e32df90695b35b..7e99eca355b52e 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
@@ -15,7 +15,12 @@ import { getCSSRules } from '@wordpress/style-engine';
 /**
  * Internal dependencies
  */
-import { PRESET_METADATA, ROOT_BLOCK_SELECTOR, scopeSelector } from './utils';
+import {
+	PRESET_METADATA,
+	ROOT_BLOCK_SELECTOR,
+	scopeSelector,
+	appendToSelector,
+} from './utils';
 import { getBlockCSSSelector } from './get-block-css-selector';
 import {
 	getTypographyFontSizeValue,
@@ -1124,18 +1129,33 @@ function updateConfigWithSeparator( config ) {
 	return config;
 }
 
-const processCSSNesting = ( css, blockSelector ) => {
+export function processCSSNesting( css, blockSelector ) {
 	let processedCSS = '';
 
 	// 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.trim() }}`;
+		} 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 combinedSelector = nestedSelector.startsWith( ' ' )
+				? scopeSelector( blockSelector, nestedSelector )
+				: appendToSelector( blockSelector, nestedSelector );
+
+			processedCSS += `${ combinedSelector }{${ cssValue.trim() }}`;
+		}
 	} );
 	return processedCSS;
-};
+}
 
 /**
  * Returns the global styles output using a global styles configuration.
diff --git a/packages/block-editor/src/components/global-styles/utils.js b/packages/block-editor/src/components/global-styles/utils.js
index d4f2d959a33659..f4adb7a7903122 100644
--- a/packages/block-editor/src/components/global-styles/utils.js
+++ b/packages/block-editor/src/components/global-styles/utils.js
@@ -393,6 +393,27 @@ export function scopeSelector( scope, selector ) {
 	return selectorsScoped.join( ', ' );
 }
 
+/**
+ * Appends a sub-selector to an existing one.
+ *
+ * Given the compounded `selector` "h1, h2, h3"
+ * and the `toAppend` selector ".some-class" the result will be
+ * "h1.some-class, h2.some-class, h3.some-class".
+ *
+ * @param {string} selector Original selector.
+ * @param {string} toAppend Selector to append.
+ *
+ * @return {string} The new selector.
+ */
+export function appendToSelector( selector, toAppend ) {
+	if ( ! selector.includes( ',' ) ) {
+		return selector + toAppend;
+	}
+	const selectors = selector.split( ',' );
+	const newSelectors = selectors.map( ( sel ) => sel + toAppend );
+	return newSelectors.join( ',' );
+}
+
 /**
  * Compares global style variations according to their styles and settings properties.
  *
diff --git a/phpunit/class-wp-theme-json-test.php b/phpunit/class-wp-theme-json-test.php
index 39f308a5791f60..0e212983d9080f 100644
--- a/phpunit/class-wp-theme-json-test.php
+++ b/phpunit/class-wp-theme-json-test.php
@@ -2007,29 +2007,37 @@ public function test_process_blocks_custom_css( $input, $expected ) {
 	 */
 	public function data_process_blocks_custom_css() {
 		return array(
-			// Simple CSS without any child selectors.
-			'no child selectors'                => array(
+			// Simple CSS without any nested selectors.
+			'no nested selectors'          => array(
 				'input'    => array(
 					'selector' => '.foo',
 					'css'      => 'color: red; margin: auto;',
 				),
 				'expected' => '.foo{color: red; margin: auto;}',
 			),
-			// CSS with child selectors.
-			'with children'                     => array(
+			// CSS with nested selectors.
+			'with nested selector'         => array(
 				'input'    => array(
 					'selector' => '.foo',
-					'css'      => 'color: red; margin: auto; & .bar{color: blue;}',
+					'css'      => 'color: red; margin: auto; &.one{color: blue;} & .two{color: green;}',
 				),
-				'expected' => '.foo{color: red; margin: auto;}.foo .bar{color: blue;}',
+				'expected' => '.foo{color: red; margin: auto;}.foo.one{color: blue;}.foo .two{color: green;}',
 			),
-			// CSS with child selectors and pseudo elements.
-			'with children and pseudo elements' => array(
+			// CSS with pseudo elements.
+			'with pseudo elements'         => array(
 				'input'    => array(
 					'selector' => '.foo',
-					'css'      => 'color: red; margin: auto; & .bar{color: blue;} &::before{color: green;}',
+					'css'      => 'color: red; margin: auto; &::before{color: blue;} & ::before{color: green;}  &.one::before{color: yellow;} & .two::before{color: purple;}',
 				),
-				'expected' => '.foo{color: red; margin: auto;}.foo .bar{color: blue;}.foo::before{color: green;}',
+				'expected' => '.foo{color: red; margin: auto;}.foo::before{color: blue;}.foo ::before{color: green;}.foo.one::before{color: yellow;}.foo .two::before{color: purple;}',
+			),
+			// CSS with multiple root selectors.
+			'with multiple root selectors' => array(
+				'input'    => array(
+					'selector' => '.foo, .bar',
+					'css'      => 'color: red; margin: auto; &.one{color: blue;} & .two{color: green;} &::before{color: yellow;} & ::before{color: purple;}  &.three::before{color: orange;} & .four::before{color: skyblue;}',
+				),
+				'expected' => '.foo, .bar{color: red; margin: auto;}.foo.one, .bar.one{color: blue;}.foo .two, .bar .two{color: green;}.foo::before, .bar::before{color: yellow;}.foo ::before, .bar ::before{color: purple;}.foo.three::before, .bar.three::before{color: orange;}.foo .four::before, .bar .four::before{color: skyblue;}',
 			),
 		);
 	}