diff --git a/src/wp-includes/script-loader.php b/src/wp-includes/script-loader.php
index 801da32c21..44e9263b78 100644
--- a/src/wp-includes/script-loader.php
+++ b/src/wp-includes/script-loader.php
@@ -2701,6 +2701,7 @@ function wp_maybe_inline_styles() {
 		if ( wp_styles()->get_data( $handle, 'path' ) && file_exists( $wp_styles->registered[ $handle ]->extra['path'] ) ) {
 			$styles[] = array(
 				'handle' => $handle,
+				'src'    => $wp_styles->registered[ $handle ]->src,
 				'path'   => $wp_styles->registered[ $handle ]->extra['path'],
 				'size'   => filesize( $wp_styles->registered[ $handle ]->extra['path'] ),
 			);
@@ -2735,6 +2736,10 @@ function wp_maybe_inline_styles() {
 			// Get the styles if we don't already have them.
 			$style['css'] = file_get_contents( $style['path'] );
 
+			// Check if the style contains relative URLs that need to be modified.
+			// URLs relative to the stylesheet's path should be converted to relative to the site's root.
+			$style['css'] = _wp_normalize_relative_css_links( $style['css'], $style['src'] );
+
 			// Set `src` to `false` and add styles inline.
 			$wp_styles->registered[ $style['handle'] ]->src = false;
 			if ( empty( $wp_styles->registered[ $style['handle'] ]->extra['after'] ) ) {
@@ -2748,6 +2753,45 @@ function wp_maybe_inline_styles() {
 	}
 }
 
+/**
+ * Make URLs relative to the WordPress installation.
+ *
+ * @since 5.9.0
+ * @access private
+ *
+ * @param string $css            The CSS to make URLs relative to the WordPress installation.
+ * @param string $stylesheet_url The URL to the stylesheet.
+ *
+ * @return string The CSS with URLs made relative to the WordPress installation.
+ */
+function _wp_normalize_relative_css_links( $css, $stylesheet_url ) {
+	$has_src_results = preg_match_all( '#url\s*\(\s*[\'"]?\s*([^\'"\)]+)#', $css, $src_results );
+	if ( $has_src_results ) {
+		// Loop through the URLs to find relative ones.
+		foreach ( $src_results[1] as $src_index => $src_result ) {
+			// Skip if this is an absolute URL.
+			if ( 0 === strpos( $src_result, 'http' ) || 0 === strpos( $src_result, '//' ) ) {
+				continue;
+			}
+
+			// Build the absolute URL.
+			$absolute_url = dirname( $stylesheet_url ) . '/' . $src_result;
+			$absolute_url = str_replace( '/./', '/', $absolute_url );
+			// Convert to URL related to the site root.
+			$relative_url = wp_make_link_relative( $absolute_url );
+
+			// Replace the URL in the CSS.
+			$css = str_replace(
+				$src_results[0][ $src_index ],
+				str_replace( $src_result, $relative_url, $src_results[0][ $src_index ] ),
+				$css
+			);
+		}
+	}
+
+	return $css;
+}
+
 /**
  * Inject the block editor assets that need to be loaded into the editor's iframe as an inline script.
  *
diff --git a/tests/phpunit/tests/dependencies/styles.php b/tests/phpunit/tests/dependencies/styles.php
index f5eed18758..bec55ac032 100644
--- a/tests/phpunit/tests/dependencies/styles.php
+++ b/tests/phpunit/tests/dependencies/styles.php
@@ -189,6 +189,51 @@ class Tests_Dependencies_Styles extends WP_UnitTestCase {
 
 	}
 
+	/**
+	 * Test normalizing relative links in CSS.
+	 *
+	 * @dataProvider data_normalize_relative_css_links
+	 *
+	 * @ticket 54243
+	 *
+	 * @covers ::_wp_normalize_relative_css_links
+	 *
+	 * @param string $css      Given CSS to test.
+	 * @param string $expected Expected result.
+	 */
+	public function test_normalize_relative_css_links( $css, $expected ) {
+		$this->assertSame(
+			$expected,
+			_wp_normalize_relative_css_links( $css, site_url( 'wp-content/themes/test/style.css' ) )
+		);
+	}
+
+	/**
+	 * Data provider.
+	 *
+	 * @return array
+	 */
+	public function data_normalize_relative_css_links() {
+		return array(
+			'Double quotes, same path'                     => array(
+				'css'      => 'p {background:url( "image0.svg" );}',
+				'expected' => 'p {background:url( "/wp-content/themes/test/image0.svg" );}',
+			),
+			'Single quotes, same path, prefixed with "./"' => array(
+				'css'      => 'p {background-image: url(\'./image2.png\');}',
+				'expected' => 'p {background-image: url(\'/wp-content/themes/test/image2.png\');}',
+			),
+			'Single quotes, one level up, prefixed with "../"' => array(
+				'css'      => 'p {background-image: url(\'../image1.jpg\');}',
+				'expected' => 'p {background-image: url(\'/wp-content/themes/test/../image1.jpg\');}',
+			),
+			'External URLs, shouldn\'t change'             => array(
+				'css'      => 'p {background-image: url(\'http://foo.com/image2.png\');}',
+				'expected' => 'p {background-image: url(\'http://foo.com/image2.png\');}',
+			),
+		);
+	}
+
 	/**
 	 * Test if multiple inline styles work
 	 *