diff --git a/src/wp-includes/blocks.php b/src/wp-includes/blocks.php
index 4d3ad3d4bd..31f1b22469 100644
--- a/src/wp-includes/blocks.php
+++ b/src/wp-includes/blocks.php
@@ -445,11 +445,13 @@ function register_block_type_from_metadata( $file_or_folder, $args = array() ) {
 	 * Using a static variable ensures that the metadata is only read once per request.
 	 */
 
+	$file_or_folder = wp_normalize_path( $file_or_folder );
+
 	$metadata_file = ( ! str_ends_with( $file_or_folder, 'block.json' ) ) ?
 		trailingslashit( $file_or_folder ) . 'block.json' :
 		$file_or_folder;
 
-	$is_core_block        = str_starts_with( $file_or_folder, ABSPATH . WPINC );
+	$is_core_block        = str_starts_with( $file_or_folder, wp_normalize_path( ABSPATH . WPINC ) );
 	$metadata_file_exists = $is_core_block || file_exists( $metadata_file );
 	$registry_metadata    = WP_Block_Metadata_Registry::get_metadata( $file_or_folder );
 
diff --git a/src/wp-includes/class-wp-block-metadata-registry.php b/src/wp-includes/class-wp-block-metadata-registry.php
index e7e71afcd1..cba8193b7e 100644
--- a/src/wp-includes/class-wp-block-metadata-registry.php
+++ b/src/wp-includes/class-wp-block-metadata-registry.php
@@ -82,7 +82,7 @@ class WP_Block_Metadata_Registry {
 	 * @return bool True if the collection was registered successfully, false otherwise.
 	 */
 	public static function register_collection( $path, $manifest ) {
-		$path = wp_normalize_path( rtrim( $path, '/' ) );
+		$path = rtrim( wp_normalize_path( $path ), '/' );
 
 		$collection_roots = self::get_default_collection_roots();
 
@@ -112,7 +112,7 @@ class WP_Block_Metadata_Registry {
 		$collection_roots = array_unique(
 			array_map(
 				static function ( $allowed_root ) {
-					return rtrim( $allowed_root, '/' );
+					return rtrim( wp_normalize_path( $allowed_root ), '/' );
 				},
 				$collection_roots
 			)
@@ -161,6 +161,8 @@ class WP_Block_Metadata_Registry {
 	 * @return array|null The block metadata for the block, or null if not found.
 	 */
 	public static function get_metadata( $file_or_folder ) {
+		$file_or_folder = wp_normalize_path( $file_or_folder );
+
 		$path = self::find_collection_path( $file_or_folder );
 		if ( ! $path ) {
 			return null;
@@ -194,7 +196,7 @@ class WP_Block_Metadata_Registry {
 	 * @return string[] List of block metadata file paths, or an empty array if the given `$path` is invalid.
 	 */
 	public static function get_collection_block_metadata_files( $path ) {
-		$path = wp_normalize_path( rtrim( $path, '/' ) );
+		$path = rtrim( wp_normalize_path( $path ), '/' );
 
 		if ( ! isset( self::$collections[ $path ] ) ) {
 			_doing_it_wrong(
@@ -213,6 +215,7 @@ class WP_Block_Metadata_Registry {
 		}
 
 		return array_map(
+			// No normalization necessary since `$path` is already normalized and `$block_name` is just a folder name.
 			static function ( $block_name ) use ( $path ) {
 				return "{$path}/{$block_name}/block.json";
 			},
@@ -225,8 +228,8 @@ class WP_Block_Metadata_Registry {
 	 *
 	 * @since 6.7.0
 	 *
-	 * @param string $file_or_folder The path to the file or folder.
-	 * @return string|null The collection path if found, or null if not found.
+	 * @param string $file_or_folder The normalized path to the file or folder.
+	 * @return string|null The normalized collection path if found, or null if not found.
 	 */
 	private static function find_collection_path( $file_or_folder ) {
 		if ( empty( $file_or_folder ) ) {
@@ -234,7 +237,7 @@ class WP_Block_Metadata_Registry {
 		}
 
 		// Check the last matched collection first, since block registration usually happens in batches per plugin or theme.
-		$path = wp_normalize_path( rtrim( $file_or_folder, '/' ) );
+		$path = rtrim( $file_or_folder, '/' );
 		if ( self::$last_matched_collection && str_starts_with( $path, self::$last_matched_collection ) ) {
 			return self::$last_matched_collection;
 		}
@@ -279,7 +282,7 @@ class WP_Block_Metadata_Registry {
 	 *
 	 * @since 6.7.0
 	 *
-	 * @param string $path The file or folder path to determine the block identifier from.
+	 * @param string $path The normalized file or folder path to determine the block identifier from.
 	 * @return string The block identifier, or an empty string if the path is empty.
 	 */
 	private static function default_identifier_callback( $path ) {
@@ -302,8 +305,8 @@ class WP_Block_Metadata_Registry {
 	 *
 	 * @since 6.7.2
 	 *
-	 * @param string   $path             Block metadata collection path, without trailing slash.
-	 * @param string[] $collection_roots List of collection root paths, without trailing slashes.
+	 * @param string   $path             Normalized block metadata collection path, without trailing slash.
+	 * @param string[] $collection_roots List of normalized collection root paths, without trailing slashes.
 	 * @return bool True if the path is allowed, false otherwise.
 	 */
 	private static function is_valid_collection_path( $path, $collection_roots ) {
diff --git a/tests/phpunit/tests/blocks/register.php b/tests/phpunit/tests/blocks/register.php
index 7e0c391e1f..8e0b6a6409 100644
--- a/tests/phpunit/tests/blocks/register.php
+++ b/tests/phpunit/tests/blocks/register.php
@@ -1501,4 +1501,15 @@ class Tests_Blocks_Register extends WP_UnitTestCase {
 			$block_type->block_hooks
 		);
 	}
+
+	/**
+	 * @ticket 63027
+	 *
+	 * @covers ::register_block_type_from_metadata
+	 */
+	public function test_register_block_type_from_metadata_with_windows_path() {
+		$windows_like_path = str_replace( '/', '\\', DIR_TESTDATA ) . '\\blocks\\notice';
+
+		$this->assertNotFalse( register_block_type_from_metadata( $windows_like_path ) );
+	}
 }
diff --git a/tests/phpunit/tests/blocks/wpBlockMetadataRegistry.php b/tests/phpunit/tests/blocks/wpBlockMetadataRegistry.php
index 6c3fd5e277..4a1ddb3c94 100644
--- a/tests/phpunit/tests/blocks/wpBlockMetadataRegistry.php
+++ b/tests/phpunit/tests/blocks/wpBlockMetadataRegistry.php
@@ -220,4 +220,72 @@ class Tests_Blocks_WpBlockMetadataRegistry extends WP_UnitTestCase {
 			WP_Block_Metadata_Registry::get_collection_block_metadata_files( $path )
 		);
 	}
+
+	/**
+	 * Tests that `register_collection()`, `get_metadata()`, and `get_collection_metadata_files()` handle Windows paths.
+	 *
+	 * @ticket 63027
+	 * @covers ::register_collection
+	 * @covers ::get_metadata
+	 * @covers ::get_collection_metadata_files
+	 */
+	public function test_with_windows_paths() {
+		// Set up a mock manifest file.
+		$manifest_data = array(
+			'test-block' => array(
+				'name'  => 'test-block',
+				'title' => 'Test Block',
+			),
+		);
+		file_put_contents( $this->temp_manifest_file, '<?php return ' . var_export( $manifest_data, true ) . ';' );
+
+		$plugins_path = 'C:\\Site\\wp-content\\plugins';
+		$plugin_path  = $plugins_path . '\\my-plugin\\blocks';
+		$block_path   = $plugin_path . '\\test-block\\block.json';
+
+		// Register the mock plugins directory as an allowed root.
+		add_filter(
+			'wp_allowed_block_metadata_collection_roots',
+			static function ( $paths ) use ( $plugins_path ) {
+				$paths[] = $plugins_path;
+				return $paths;
+			}
+		);
+
+		$this->assertTrue( WP_Block_Metadata_Registry::register_collection( $plugin_path, $this->temp_manifest_file ), 'Could not register block metadata collection.' );
+		$this->assertSame( $manifest_data['test-block'], WP_Block_Metadata_Registry::get_metadata( $block_path ), 'Could not find collection for provided block.json path.' );
+		$this->assertSame( array( wp_normalize_path( $block_path ) ), WP_Block_Metadata_Registry::get_collection_block_metadata_files( $plugin_path ), 'Could not get correct list of block.json paths for collection.' );
+	}
+
+	/**
+	 * Tests that `register_collection()` handles Windows paths correctly for verifying allowed roots.
+	 *
+	 * @ticket 63027
+	 * @covers ::register_collection
+	 */
+	public function test_with_windows_paths_and_disallowed_location() {
+		$parent_path  = 'C:\\Site\\wp-content';
+		$plugins_path = $parent_path . '\\plugins';
+		$plugin_path  = $plugins_path . '\\my-plugin\\blocks';
+
+		// Register the mock plugins directory as an allowed root.
+		add_filter(
+			'wp_allowed_block_metadata_collection_roots',
+			static function ( $paths ) use ( $plugins_path ) {
+				$paths[] = $plugins_path;
+				return $paths;
+			}
+		);
+
+		$this->setExpectedIncorrectUsage( 'WP_Block_Metadata_Registry::register_collection' );
+
+		$result = WP_Block_Metadata_Registry::register_collection( $plugins_path, $this->temp_manifest_file );
+		$this->assertFalse( $result, 'Arbitrary Windows path should not be registered if it matches a collection root' );
+
+		$result = WP_Block_Metadata_Registry::register_collection( $parent_path, $this->temp_manifest_file );
+		$this->assertFalse( $result, 'Arbitrary Windows path should not be registered if it is a parent directory of a collection root' );
+
+		$result = WP_Block_Metadata_Registry::register_collection( $plugin_path, $this->temp_manifest_file );
+		$this->assertTrue( $result, 'Arbitrary Windows path should be registered successfully if it is within a collection root' );
+	}
 }