diff --git a/src/wp-includes/class-wp-block-metadata-registry.php b/src/wp-includes/class-wp-block-metadata-registry.php
index 2214e98d10db7..2707fe9a36fdd 100644
--- a/src/wp-includes/class-wp-block-metadata-registry.php
+++ b/src/wp-includes/class-wp-block-metadata-registry.php
@@ -53,6 +53,14 @@ class WP_Block_Metadata_Registry {
 	 */
 	private static $plugin_dir = '';
 
+	/**
+	 * Stores the normalized WordPress theme directory path.
+	 *
+	 * @since 6.7.0
+	 * @var string
+	 */
+	private static $theme_dir = '';
+
 	/**
 	 * Registers a block metadata collection.
 	 *
@@ -94,6 +102,7 @@ public static function register_collection( $path, $manifest ) {
 
 		$wpinc_path = self::get_include_path();
 		$plugin_dir = self::get_plugin_dir();
+		$theme_dir  = self::get_theme_dir();
 
 		// Check if the path is valid:
 		if ( str_starts_with( $path, $wpinc_path ) ) {
@@ -106,15 +115,17 @@ public static function register_collection( $path, $manifest ) {
 			if ( empty( $plugin_name ) || $plugin_name === $relative_path ) {
 				_doing_it_wrong(
 					__METHOD__,
-					__( 'Block metadata collections can only be registered for a specific plugin. The provided path is neither a core path nor a valid plugin path.' ),
+					__( 'Block metadata collections can only be registered for a specific plugin or theme. The provided path is neither a core path, a valid plugin path, nor a valid theme path.' ),
 					'6.7.0'
 				);
 				return false;
 			}
+		} elseif ( str_starts_with( $path, $theme_dir ) ) {
+			// Theme path is valid.
 		} else {
 			_doing_it_wrong(
 				__METHOD__,
-				__( 'Block metadata collections can only be registered for a specific plugin. The provided path is neither a core path nor a valid plugin path.' ),
+				__( 'Block metadata collections can only be registered for a specific plugin or theme. The provided path is neither a core path, a valid plugin path, nor a valid theme path.' ),
 				'6.7.0'
 			);
 			return false;
@@ -271,4 +282,18 @@ private static function get_plugin_dir() {
 		}
 		return self::$plugin_dir;
 	}
+
+	/**
+	 * Gets the normalized WordPress theme directory path.
+	 *
+	 * @since 6.7.0
+	 *
+	 * @return string The normalized WordPress theme directory path.
+	 */
+	private static function get_theme_dir() {
+		if ( empty( self::$theme_dir ) ) {
+			self::$theme_dir = wp_normalize_path( get_theme_root() );
+		}
+		return self::$theme_dir;
+	}
 }
diff --git a/tests/phpunit/tests/blocks/registerBlockTypeFromMetadataWithRegistry.php b/tests/phpunit/tests/blocks/registerBlockTypeFromMetadataWithRegistry.php
index b778a3fb5c838..335d07dd08c6d 100644
--- a/tests/phpunit/tests/blocks/registerBlockTypeFromMetadataWithRegistry.php
+++ b/tests/phpunit/tests/blocks/registerBlockTypeFromMetadataWithRegistry.php
@@ -91,6 +91,66 @@ public function test_register_block_type_from_metadata_with_registry_and_overrid
 		$this->assertEquals( array( 'html' => true ), $registered_block->supports );
 	}
 
+	public function test_register_block_type_from_metadata_with_registry_in_parent_theme() {
+		$parent_theme_path = get_theme_root() . '/twentytwentyone';
+		$block_json_path   = $parent_theme_path . '/blocks/test-block/block.json';
+
+		// Create a manifest file with metadata for our test block
+		$manifest_data = array(
+			'test-block' => array(
+				'name'        => 'twentytwentyone/test-block',
+				'title'       => 'Parent Theme Test Block',
+				'category'    => 'widgets',
+				'icon'        => 'smiley',
+				'description' => 'A test block registered via WP_Block_Metadata_Registry in the parent theme',
+				'supports'    => array( 'html' => false ),
+				'textdomain'  => 'twentytwentyone',
+			),
+		);
+		file_put_contents( $this->temp_manifest_file, '<?php return ' . var_export( $manifest_data, true ) . ';' );
+
+		// Register the collection
+		WP_Block_Metadata_Registry::register_collection( $parent_theme_path . '/blocks', $this->temp_manifest_file );
+
+		// Attempt to register the block
+		$registered_block = register_block_type_from_metadata( $block_json_path );
+
+		// Assert that the block was registered successfully
+		$this->assertInstanceOf( 'WP_Block_Type', $registered_block );
+		$this->assertEquals( 'twentytwentyone/test-block', $registered_block->name );
+		$this->assertEquals( 'Parent Theme Test Block', $registered_block->title );
+	}
+
+	public function test_register_block_type_from_metadata_with_registry_in_child_theme() {
+		$child_theme_path = get_theme_root() . '/twentytwentyone-child';
+		$block_json_path  = $child_theme_path . '/blocks/test-block/block.json';
+
+		// Create a manifest file with metadata for our test block
+		$manifest_data = array(
+			'test-block' => array(
+				'name'        => 'twentytwentyone-child/test-block',
+				'title'       => 'Child Theme Test Block',
+				'category'    => 'widgets',
+				'icon'        => 'smiley',
+				'description' => 'A test block registered via WP_Block_Metadata_Registry in the child theme',
+				'supports'    => array( 'html' => false ),
+				'textdomain'  => 'twentytwentyone-child',
+			),
+		);
+		file_put_contents( $this->temp_manifest_file, '<?php return ' . var_export( $manifest_data, true ) . ';' );
+
+		// Register the collection
+		WP_Block_Metadata_Registry::register_collection( $child_theme_path . '/blocks', $this->temp_manifest_file );
+
+		// Attempt to register the block
+		$registered_block = register_block_type_from_metadata( $block_json_path );
+
+		// Assert that the block was registered successfully
+		$this->assertInstanceOf( 'WP_Block_Type', $registered_block );
+		$this->assertEquals( 'twentytwentyone-child/test-block', $registered_block->name );
+		$this->assertEquals( 'Child Theme Test Block', $registered_block->title );
+	}
+
 	private function unregister_test_blocks() {
 		$registry   = WP_Block_Type_Registry::get_instance();
 		$block_name = 'test-suite/test-block';
diff --git a/tests/phpunit/tests/blocks/wpBlockMetadataRegistry.php b/tests/phpunit/tests/blocks/wpBlockMetadataRegistry.php
index 3f0ec006b0a0a..dabfcb7a6bfc9 100644
--- a/tests/phpunit/tests/blocks/wpBlockMetadataRegistry.php
+++ b/tests/phpunit/tests/blocks/wpBlockMetadataRegistry.php
@@ -88,4 +88,20 @@ public function test_register_collection_with_non_existent_path() {
 		$result = WP_Block_Metadata_Registry::register_collection( $non_existent_path, $this->temp_manifest_file );
 		$this->assertFalse( $result, 'Non-existent path should not be registered' );
 	}
+
+	public function test_register_collection_with_valid_theme_path() {
+		$valid_theme_path = get_theme_root() . '/mytheme/blocks';
+
+		$result = WP_Block_Metadata_Registry::register_collection( $valid_theme_path, $this->temp_manifest_file );
+		$this->assertTrue( $result, 'Valid theme path should be registered successfully' );
+	}
+
+	public function test_register_collection_with_invalid_theme_path() {
+		$invalid_plugin_path = get_theme_root();
+
+		$this->setExpectedIncorrectUsage( 'WP_Block_Metadata_Registry::register_collection' );
+
+		$result = WP_Block_Metadata_Registry::register_collection( $invalid_plugin_path, $this->temp_manifest_file );
+		$this->assertFalse( $result, 'Invalid theme path should not be registered' );
+	}
 }