diff --git a/src/wp-includes/blocks.php b/src/wp-includes/blocks.php
index 5fa7f1d6d0ddc..7b96ebc2ba9c6 100644
--- a/src/wp-includes/blocks.php
+++ b/src/wp-includes/blocks.php
@@ -373,6 +373,12 @@ function register_block_type_from_metadata( $file_or_folder, $args = array() ) {
 		if ( ! isset( $metadata['style'] ) ) {
 			$metadata['style'] = "wp-block-$block_name";
 		}
+
+		if ( current_theme_supports( 'wp-block-styles' ) && wp_should_load_separate_core_block_assets() ) {
+			$metadata['style']   = (array) $metadata['style'];
+			$metadata['style'][] = "wp-block-{$block_name}-theme";
+		}
+
 		if ( ! isset( $metadata['editorStyle'] ) ) {
 			$metadata['editorStyle'] = "wp-block-{$block_name}-editor";
 		}
diff --git a/src/wp-includes/blocks/index.php b/src/wp-includes/blocks/index.php
index 49bf114393b6a..403930c5ca55b 100644
--- a/src/wp-includes/blocks/index.php
+++ b/src/wp-includes/blocks/index.php
@@ -40,6 +40,10 @@ function register_core_block_style_handles() {
 		'editorStyle' => 'editor',
 	);
 
+	if( current_theme_supports( 'wp-block-styles' ) ){
+		$style_fields['themeStyle'] = 'theme';
+	}
+
 	/*
 	 * Ignore transient cache when `WP_DEBUG` is enabled. Why? To avoid interfering with
 	 * the core developer's workflow.
@@ -68,6 +72,9 @@ function register_core_block_style_handles() {
 		if ( ! isset( $schema['editorStyle'] ) ) {
 			$schema['editorStyle'] = "wp-block-{$name}-editor";
 		}
+		if ( ! isset( $schema['themeStyle'] ) ) {
+			$schema['themeStyle'] = "wp-block-{$name}-theme";
+		}
 
 		foreach ( $style_fields as $style_field => $filename ) {
 			$style_handle = $schema[ $style_field ];
diff --git a/src/wp-includes/script-loader.php b/src/wp-includes/script-loader.php
index 3ee28ce23c9d4..168e88d2e5809 100644
--- a/src/wp-includes/script-loader.php
+++ b/src/wp-includes/script-loader.php
@@ -2372,20 +2372,8 @@ function wp_common_block_scripts_and_styles() {
 
 	wp_enqueue_style( 'wp-block-library' );
 
-	if ( current_theme_supports( 'wp-block-styles' ) ) {
-		if ( wp_should_load_separate_core_block_assets() ) {
-			$suffix = defined( 'SCRIPT_DEBUG' ) && SCRIPT_DEBUG ? 'css' : 'min.css';
-			$files  = glob( __DIR__ . "/blocks/**/theme.$suffix" );
-			foreach ( $files as $path ) {
-				$block_name = basename( dirname( $path ) );
-				if ( is_rtl() && file_exists( __DIR__ . "/blocks/$block_name/theme-rtl.$suffix" ) ) {
-					$path = __DIR__ . "/blocks/$block_name/theme-rtl.$suffix";
-				}
-				wp_add_inline_style( "wp-block-{$block_name}", file_get_contents( $path ) );
-			}
-		} else {
-			wp_enqueue_style( 'wp-block-library-theme' );
-		}
+	if ( current_theme_supports( 'wp-block-styles' ) && ! wp_should_load_separate_core_block_assets() ) {
+		wp_enqueue_style( 'wp-block-library-theme' );
 	}
 
 	/**
diff --git a/tests/phpunit/tests/blocks/registerCoreBlockStyleHandles.php b/tests/phpunit/tests/blocks/registerCoreBlockStyleHandles.php
index 0f11962248bf2..7edd1d4f25c28 100644
--- a/tests/phpunit/tests/blocks/registerCoreBlockStyleHandles.php
+++ b/tests/phpunit/tests/blocks/registerCoreBlockStyleHandles.php
@@ -99,6 +99,39 @@ public function test_wp_should_load_separate_core_block_assets_true( $name, $sch
 		}
 	}
 
+	/**
+	 * @ticket 58528
+	 *
+	 * @dataProvider data_block_data
+	 */
+	public function test_wp_should_load_separate_core_block_assets_current_theme_supports( $name, $schema ) {
+		add_filter( 'should_load_separate_core_block_assets', '__return_true' );
+		add_theme_support( 'wp-block-styles' );
+		register_core_block_style_handles();
+
+		$wp_styles = $GLOBALS['wp_styles'];
+
+		$style_fields               = self::STYLE_FIELDS;
+		$style_fields['themeStyle'] = 'theme';
+
+		foreach ( $style_fields as $style_field => $filename ) {
+			$style_handle = $schema[ $style_field ];
+			if ( is_array( $style_handle ) ) {
+				continue;
+			}
+
+			$this->assertArrayHasKey( $style_handle, $wp_styles->registered, 'The key should exist, as this style should be registered' );
+			if ( false === $wp_styles->registered[ $style_handle ]->src ) {
+				$this->assertEmpty( $wp_styles->registered[ $style_handle ]->extra, 'If source is false, not style path should be set' );
+			} else {
+				$this->assertStringContainsString( $this->includes_url, $wp_styles->registered[ $style_handle ]->src, 'Source of style should contain the includes url' );
+				$this->assertNotEmpty( $wp_styles->registered[ $style_handle ]->extra, 'The path of the style should exist' );
+				$this->assertArrayHasKey( 'path', $wp_styles->registered[ $style_handle ]->extra, 'The path key of the style should exist in extra array' );
+				$this->assertNotEmpty( $wp_styles->registered[ $style_handle ]->extra['path'], 'The path key of the style should not be empty' );
+			}
+		}
+	}
+
 
 	public function data_block_data() {
 		$core_blocks_meta = require ABSPATH . WPINC . '/blocks/blocks-json.php';
@@ -112,6 +145,10 @@ public function data_block_data() {
 				$schema['editorStyle'] = "wp-block-{$name}-editor";
 			}
 
+			if ( ! isset( $schema['themeStyle'] ) ) {
+				$schema['themeStyle'] = "wp-block-{$name}-theme";
+			}
+
 			$data[ $name ] = array( $name, $schema );
 		}