diff --git a/src/wp-includes/class-wp-theme-json.php b/src/wp-includes/class-wp-theme-json.php
index 631dd1f703e67..c1270055e010d 100644
--- a/src/wp-includes/class-wp-theme-json.php
+++ b/src/wp-includes/class-wp-theme-json.php
@@ -1445,9 +1445,16 @@ public function get_stylesheet( $types = array( 'variables', 'styles', 'presets'
 	protected function process_blocks_custom_css( $css, $selector ) {
 		$processed_css = '';
 
+		if ( empty( $css ) ) {
+			return $processed_css;
+		}
+
 		// Split CSS nested rules.
 		$parts = explode( '&', $css );
 		foreach ( $parts as $part ) {
+			if ( empty( $part ) ) {
+				continue;
+			}
 			$is_root_css = ( ! str_contains( $part, '{' ) );
 			if ( $is_root_css ) {
 				// If the part doesn't contain braces, it applies to the root level.
@@ -1460,11 +1467,25 @@ protected function process_blocks_custom_css( $css, $selector ) {
 				}
 				$nested_selector = $part[0];
 				$css_value       = $part[1];
-				$part_selector   = str_starts_with( $nested_selector, ' ' )
+
+				/*
+				 * Handle pseudo elements such as ::before, ::after etc. Regex will also
+				 * capture any leading combinator such as >, +, or ~, as well as spaces.
+				 * This allows pseudo elements as descendants e.g. `.parent ::before`.
+				 */
+				$matches            = array();
+				$has_pseudo_element = preg_match( '/([>+~\s]*::[a-zA-Z-]+)/', $nested_selector, $matches );
+				$pseudo_part        = $has_pseudo_element ? $matches[1] : '';
+				$nested_selector    = $has_pseudo_element ? str_replace( $pseudo_part, '', $nested_selector ) : $nested_selector;
+
+				// Finalize selector and re-append pseudo element if required.
+				$part_selector  = str_starts_with( $nested_selector, ' ' )
 					? static::scope_selector( $selector, $nested_selector )
 					: static::append_to_selector( $selector, $nested_selector );
-				$final_selector  = ":root :where($part_selector)";
-				$processed_css  .= $final_selector . '{' . trim( $css_value ) . '}';}
+				$final_selector = ":root :where($part_selector)$pseudo_part";
+
+				$processed_css .= $final_selector . '{' . trim( $css_value ) . '}';
+			}
 		}
 		return $processed_css;
 	}
diff --git a/tests/phpunit/tests/theme/wpThemeJson.php b/tests/phpunit/tests/theme/wpThemeJson.php
index bc8ef8121ddd0..ac56c16ef3baf 100644
--- a/tests/phpunit/tests/theme/wpThemeJson.php
+++ b/tests/phpunit/tests/theme/wpThemeJson.php
@@ -5224,6 +5224,7 @@ public function data_custom_css_for_user_caps() {
 
 	/**
 	 * @ticket 61165
+	 * @ticket 61769
 	 *
 	 * @dataProvider data_process_blocks_custom_css
 	 *
@@ -5251,6 +5252,13 @@ public function test_process_blocks_custom_css( $input, $expected ) {
 	public function data_process_blocks_custom_css() {
 		return array(
 			// Simple CSS without any nested selectors.
+			'empty css'                    => array(
+				'input'    => array(
+					'selector' => '.foo',
+					'css'      => '',
+				),
+				'expected' => '',
+			),
 			'no nested selectors'          => array(
 				'input'    => array(
 					'selector' => '.foo',
@@ -5266,13 +5274,20 @@ public function data_process_blocks_custom_css() {
 				),
 				'expected' => ':root :where(.foo){color: red; margin: auto;}:root :where(.foo.one){color: blue;}:root :where(.foo .two){color: green;}',
 			),
+			'no root styles'               => array(
+				'input'    => array(
+					'selector' => '.foo',
+					'css'      => '&::before{color: red;}',
+				),
+				'expected' => ':root :where(.foo)::before{color: red;}',
+			),
 			// CSS with pseudo elements.
 			'with pseudo elements'         => array(
 				'input'    => array(
 					'selector' => '.foo',
 					'css'      => 'color: red; margin: auto; &::before{color: blue;} & ::before{color: green;}  &.one::before{color: yellow;} & .two::before{color: purple;}',
 				),
-				'expected' => ':root :where(.foo){color: red; margin: auto;}:root :where(.foo::before){color: blue;}:root :where(.foo ::before){color: green;}:root :where(.foo.one::before){color: yellow;}:root :where(.foo .two::before){color: purple;}',
+				'expected' => ':root :where(.foo){color: red; margin: auto;}:root :where(.foo)::before{color: blue;}:root :where(.foo) ::before{color: green;}:root :where(.foo.one)::before{color: yellow;}:root :where(.foo .two)::before{color: purple;}',
 			),
 			// CSS with multiple root selectors.
 			'with multiple root selectors' => array(
@@ -5280,7 +5295,7 @@ public function data_process_blocks_custom_css() {
 					'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' => ':root :where(.foo, .bar){color: red; margin: auto;}:root :where(.foo.one, .bar.one){color: blue;}:root :where(.foo .two, .bar .two){color: green;}:root :where(.foo::before, .bar::before){color: yellow;}:root :where(.foo ::before, .bar ::before){color: purple;}:root :where(.foo.three::before, .bar.three::before){color: orange;}:root :where(.foo .four::before, .bar .four::before){color: skyblue;}',
+				'expected' => ':root :where(.foo, .bar){color: red; margin: auto;}:root :where(.foo.one, .bar.one){color: blue;}:root :where(.foo .two, .bar .two){color: green;}:root :where(.foo, .bar)::before{color: yellow;}:root :where(.foo, .bar) ::before{color: purple;}:root :where(.foo.three, .bar.three)::before{color: orange;}:root :where(.foo .four, .bar .four)::before{color: skyblue;}',
 			),
 		);
 	}