diff --git a/src/wp-includes/theme.php b/src/wp-includes/theme.php
index cd83d15d1b914..8012a5947ae67 100644
--- a/src/wp-includes/theme.php
+++ b/src/wp-includes/theme.php
@@ -428,7 +428,15 @@ function register_theme_directory( $directory ) {
 		$wp_theme_directories = array();
 	}
 
-	$untrailed = untrailingslashit( $directory );
+	/*
+	 * Normalize the path so that Windows backslashes are converted to forward
+	 * slashes. This ensures consistent path storage and comparison across
+	 * operating systems, preventing issues when a database dump made on Windows
+	 * is loaded on a Unix-based system (and vice versa).
+	 *
+	 * See https://core.trac.wordpress.org/ticket/29051
+	 */
+	$untrailed = untrailingslashit( wp_normalize_path( $directory ) );
 	if ( ! empty( $untrailed ) && ! in_array( $untrailed, $wp_theme_directories, true ) ) {
 		$wp_theme_directories[] = $untrailed;
 	}
@@ -469,8 +477,17 @@ function search_theme_directories( $force = false ) {
 	 * to use in get_theme_root().
 	 */
 	foreach ( $wp_theme_directories as $theme_root ) {
-		if ( str_starts_with( $theme_root, WP_CONTENT_DIR ) ) {
-			$relative_theme_roots[ str_replace( WP_CONTENT_DIR, '', $theme_root ) ] = $theme_root;
+		/*
+		 * Normalize the theme root path and the content directory to forward slashes
+		 * so that the prefix strip works correctly on Windows, where directory
+		 * separators may differ from those stored in WP_CONTENT_DIR.
+		 *
+		 * See https://core.trac.wordpress.org/ticket/29051
+		 */
+		$normalized_theme_root = wp_normalize_path( $theme_root );
+		$normalized_content_dir = wp_normalize_path( WP_CONTENT_DIR );
+		if ( str_starts_with( $normalized_theme_root, $normalized_content_dir ) ) {
+			$relative_theme_roots[ str_replace( $normalized_content_dir, '', $normalized_theme_root ) ] = $theme_root;
 		} else {
 			$relative_theme_roots[ $theme_root ] = $theme_root;
 		}
diff --git a/tests/phpunit/tests/theme/themeDir.php b/tests/phpunit/tests/theme/themeDir.php
index a953a04bc5533..5277787183840 100644
--- a/tests/phpunit/tests/theme/themeDir.php
+++ b/tests/phpunit/tests/theme/themeDir.php
@@ -319,4 +319,40 @@ public function test_theme_dir_slashes() {
 		rmdir( WP_CONTENT_DIR . '/themes/foo' );
 		rmdir( WP_CONTENT_DIR . '/themes/foo-themes' );
 	}
+
+	/**
+	 * @ticket 29051
+	 */
+	public function test_register_theme_directory_stores_normalized_path() {
+		@mkdir( WP_CONTENT_DIR . '/themes/custom-win-dir', 0777, true );
+
+		$dir = WP_CONTENT_DIR . '/themes/custom-win-dir';
+		register_theme_directory( $dir );
+
+		// Stored path must equal wp_normalize_path() output (no backslashes on any OS).
+		$stored = end( $GLOBALS['wp_theme_directories'] );
+		$this->assertSame( wp_normalize_path( $dir ), $stored );
+		$this->assertStringNotContainsString( '\\', $stored, 'Backslashes must not appear in registered theme dirs.' );
+
+		rmdir( WP_CONTENT_DIR . '/themes/custom-win-dir' );
+	}
+
+	/**
+	 * @ticket 29051
+	 */
+	public function test_search_theme_directories_finds_themes_under_content_dir() {
+		// self::THEME_ROOT is outside WP_CONTENT_DIR — themes there must still be found.
+		$results = search_theme_directories( true );
+
+		$this->assertIsArray( $results );
+
+		// Every result must carry a 'theme_root' key.
+		foreach ( $results as $slug => $data ) {
+			$this->assertArrayHasKey( 'theme_root', $data, "theme_root missing for slug: $slug" );
+		}
+
+		// At least one theme from self::THEME_ROOT must be present.
+		$roots = array_column( $results, 'theme_root' );
+		$this->assertContains( self::THEME_ROOT, $roots, 'Themes from non-content-dir root must be discoverable.' );
+	}
 }