diff --git a/wp-admin/includes/class-theme-upgrader.php b/wp-admin/includes/class-theme-upgrader.php
index 0a73f4b86c..4e874cd636 100644
--- a/wp-admin/includes/class-theme-upgrader.php
+++ b/wp-admin/includes/class-theme-upgrader.php
@@ -566,15 +566,28 @@ class Theme_Upgrader extends WP_Upgrader {
 			);
 		}
 
-		// If it's not a child theme, it must have at least an index.php to be legit.
-		if ( empty( $info['Template'] ) && ! file_exists( $working_directory . 'index.php' ) ) {
+		/*
+		 * Parent themes must contain an index file:
+		 * - classic themes require /index.php
+		 * - block themes require /templates/index.html or block-templates/index.html (deprecated 5.9.0).
+		 */
+		if (
+			empty( $info['Template'] ) &&
+			! file_exists( $working_directory . 'index.php' ) &&
+			! file_exists( $working_directory . 'templates/index.html' ) &&
+			! file_exists( $working_directory . 'block-templates/index.html' )
+		) {
 			return new WP_Error(
 				'incompatible_archive_theme_no_index',
 				$this->strings['incompatible_archive'],
 				sprintf(
-					/* translators: %s: index.php */
-					__( 'The theme is missing the %s file.' ),
-					'<code>index.php</code>'
+					/* translators: 1: templates/index.html, 2: index.php, 3: Documentation URL, 4: Template, 5: style.css */
+					__( 'Template is missing. Standalone themes need to have a %1$s or %2$s template file. <a href="%3$s">Child themes</a> need to have a %4$s header in the %5$s stylesheet.' ),
+					'<code>templates/index.html</code>',
+					'<code>index.php</code>',
+					__( 'https://developer.wordpress.org/themes/advanced-topics/child-themes/' ),
+					'<code>Template</code>',
+					'<code>style.css</code>'
 				)
 			);
 		}
diff --git a/wp-includes/class-wp-theme.php b/wp-includes/class-wp-theme.php
index cef5b034c6..c2398fb4eb 100644
--- a/wp-includes/class-wp-theme.php
+++ b/wp-includes/class-wp-theme.php
@@ -341,7 +341,9 @@ final class WP_Theme implements ArrayAccess {
 			$this->template = $this->stylesheet;
 			$theme_path     = $this->theme_root . '/' . $this->stylesheet;
 
-			if ( ! file_exists( $theme_path . '/templates/index.html' )
+			if (
+				! file_exists( $theme_path . '/templates/index.html' )
+				&& ! file_exists( $theme_path . '/block-templates/index.html' ) // Deprecated path support since 5.9.0.
 				&& ! file_exists( $theme_path . '/index.php' )
 			) {
 				$error_message = sprintf(
diff --git a/wp-includes/theme.php b/wp-includes/theme.php
index d511ab1a8d..55e2d13789 100644
--- a/wp-includes/theme.php
+++ b/wp-includes/theme.php
@@ -861,7 +861,9 @@ function validate_current_theme() {
 		return true;
 	}
 
-	if ( ! file_exists( get_template_directory() . '/templates/index.html' )
+	if (
+		! file_exists( get_template_directory() . '/templates/index.html' )
+		&& ! file_exists( get_template_directory() . '/block-templates/index.html' ) // Deprecated path support since 5.9.0.
 		&& ! file_exists( get_template_directory() . '/index.php' )
 	) {
 		// Invalid.
diff --git a/wp-includes/version.php b/wp-includes/version.php
index a3355b8c66..7c94a7faa9 100644
--- a/wp-includes/version.php
+++ b/wp-includes/version.php
@@ -16,7 +16,7 @@
  *
  * @global string $wp_version
  */
-$wp_version = '6.1-alpha-53414';
+$wp_version = '6.1-alpha-53416';
 
 /**
  * Holds the WordPress DB revision, increments when changes are made to the WordPress DB schema.