diff --git a/src/wp-includes/class-wp-theme-json-resolver.php b/src/wp-includes/class-wp-theme-json-resolver.php
index 16b74c8c72100..e97c31a4f5ed9 100644
--- a/src/wp-includes/class-wp-theme-json-resolver.php
+++ b/src/wp-includes/class-wp-theme-json-resolver.php
@@ -295,12 +295,10 @@ public static function get_block_data() {
 		 *
 		 * @param WP_Theme_JSON_Data Class to access and update the underlying data.
 		 */
-		$theme_json = apply_filters( 'theme_json_blocks', new WP_Theme_JSON_Data( $config, 'core' ) );
+		$theme_json = apply_filters( 'theme_json_blocks', new WP_Theme_JSON_Data( $config, 'blocks' ) );
 		$config     = $theme_json->get_data();
 
-		// Core here means it's the lower level part of the styles chain.
-		// It can be a core or a third-party block.
-		return new WP_Theme_JSON( $config, 'core' );
+		return new WP_Theme_JSON( $config, 'blocks' );
 	}
 
 	/**
diff --git a/src/wp-includes/class-wp-theme-json.php b/src/wp-includes/class-wp-theme-json.php
index 40262661e4c93..91a56936ac345 100644
--- a/src/wp-includes/class-wp-theme-json.php
+++ b/src/wp-includes/class-wp-theme-json.php
@@ -50,10 +50,12 @@ class WP_Theme_JSON {
 	 * The sources of data this object can represent.
 	 *
 	 * @since 5.8.0
+	 * @since 6.1.0 Added 'blocks'.
 	 * @var string[]
 	 */
 	const VALID_ORIGINS = array(
 		'default',
+		'blocks',
 		'theme',
 		'custom',
 	);
diff --git a/src/wp-includes/global-styles-and-settings.php b/src/wp-includes/global-styles-and-settings.php
index 1187837ed651f..da1cb97c07cee 100644
--- a/src/wp-includes/global-styles-and-settings.php
+++ b/src/wp-includes/global-styles-and-settings.php
@@ -113,15 +113,21 @@ function wp_get_global_stylesheet( $types = array() ) {
 	}
 
 	/*
-	 * If variables are part of the stylesheet,
-	 * we add them for all origins (default, theme, user).
+	 * If variables are part of the stylesheet, then add them.
 	 * This is so themes without a theme.json still work as before 5.9:
 	 * they can override the default presets.
 	 * See https://core.trac.wordpress.org/ticket/54782
 	 */
 	$styles_variables = '';
 	if ( in_array( 'variables', $types, true ) ) {
-		$styles_variables = $tree->get_stylesheet( array( 'variables' ) );
+		/*
+		 * Only use the default, theme, and custom origins. Why?
+		 * Because styles for `blocks` origin are added at a later phase
+		 * (i.e. in the render cycle). Here, only the ones in use are rendered.
+		 * @see wp_add_global_styles_for_blocks
+		 */
+		$origins          = array( 'default', 'theme', 'custom' );
+		$styles_variables = $tree->get_stylesheet( array( 'variables' ), $origins );
 		$types            = array_diff( $types, array( 'variables' ) );
 	}
 
@@ -133,6 +139,12 @@ function wp_get_global_stylesheet( $types = array() ) {
 	 */
 	$styles_rest = '';
 	if ( ! empty( $types ) ) {
+		/*
+		 * Only use the default, theme, and custom origins. Why?
+		 * Because styles for `blocks` origin are added at a later phase
+		 * (i.e. in the render cycle). Here, only the ones in use are rendered.
+		 * @see wp_add_global_styles_for_blocks
+		 */
 		$origins = array( 'default', 'theme', 'custom' );
 		if ( ! $supports_theme_json ) {
 			$origins = array( 'default' );
@@ -204,6 +216,11 @@ function wp_add_global_styles_for_blocks() {
 	foreach ( $block_nodes as $metadata ) {
 		$block_css = $tree->get_styles_for_block( $metadata );
 
+		if ( ! wp_should_load_separate_core_block_assets() ) {
+			wp_add_inline_style( 'global-styles', $block_css );
+			continue;
+		}
+
 		if ( isset( $metadata['name'] ) ) {
 			$block_name = str_replace( 'core/', '', $metadata['name'] );
 			/*
diff --git a/src/wp-includes/script-loader.php b/src/wp-includes/script-loader.php
index 9a45d9a6f5e2e..f3014a241f336 100644
--- a/src/wp-includes/script-loader.php
+++ b/src/wp-includes/script-loader.php
@@ -2409,14 +2409,11 @@ function wp_enqueue_global_styles() {
 	}
 
 	/*
-	 * If we are loading CSS for each block separately, then we can load the theme.json CSS conditionally.
+	 * If loading the CSS for each block separately, then load the theme.json CSS conditionally.
 	 * This removes the CSS from the global-styles stylesheet and adds it to the inline CSS for each block.
+	 * This filter must be registered before calling wp_get_global_stylesheet();
 	 */
-	if ( $separate_assets ) {
-		add_filter( 'theme_json_get_style_nodes', 'wp_filter_out_block_nodes' );
-		// Add each block as an inline css.
-		wp_add_global_styles_for_blocks();
-	}
+	add_filter( 'theme_json_get_style_nodes', 'wp_filter_out_block_nodes' );
 
 	$stylesheet = wp_get_global_stylesheet();
 
@@ -2427,6 +2424,9 @@ function wp_enqueue_global_styles() {
 	wp_register_style( 'global-styles', false, array(), true, true );
 	wp_add_inline_style( 'global-styles', $stylesheet );
 	wp_enqueue_style( 'global-styles' );
+
+	// Add each block as an inline css.
+	wp_add_global_styles_for_blocks();
 }
 
 /**