diff --git a/src/wp-includes/blocks.php b/src/wp-includes/blocks.php
index cc1ac60667773..04f99e4e2bf46 100644
--- a/src/wp-includes/blocks.php
+++ b/src/wp-includes/blocks.php
@@ -370,7 +370,16 @@ function register_block_style_handle( $metadata, $field_name, $index = 0 ) {
 
 		if ( is_rtl() && file_exists( $rtl_file ) ) {
 			wp_style_add_data( $style_handle_name, 'rtl', 'replace' );
-			wp_style_add_data( $style_handle_name, 'suffix', $suffix );
+			/*
+			 * Core block files use a '.min' suffix (e.g. style.min.css) when
+			 * SCRIPT_DEBUG is false, so the suffix must be stored so that
+			 * WP_Styles::do_item() can construct the correct RTL URL via str_replace.
+			 * Non-core block files registered from block.json never use a '.min'
+			 * suffix, so storing a non-empty suffix would cause str_replace() to
+			 * search for '.min.css' in a filename that only contains '.css',
+			 * silently failing to rewrite the URL to its RTL counterpart.
+			 */
+			wp_style_add_data( $style_handle_name, 'suffix', $is_core_block ? $suffix : '' );
 			wp_style_add_data( $style_handle_name, 'path', $rtl_file );
 		}
 	}
diff --git a/tests/phpunit/tests/blocks/register.php b/tests/phpunit/tests/blocks/register.php
index d2a836ba85e68..48608ade25657 100644
--- a/tests/phpunit/tests/blocks/register.php
+++ b/tests/phpunit/tests/blocks/register.php
@@ -843,6 +843,7 @@ public function test_success_register_block_style_handle() {
 	 *
 	 * @ticket 56325
 	 * @ticket 56797
+	 * @ticket 61625
 	 *
 	 * @covers ::register_block_style_handle
 	 */
@@ -890,6 +891,44 @@ public function test_register_block_style_handle_should_load_rtl_stylesheets_for
 		);
 	}
 
+	/**
+	 * Tests that register_block_style_handle() always stores an empty suffix for
+	 * non-core blocks, so that WP_Styles::do_item() can correctly rewrite the
+	 * stylesheet URL to its RTL counterpart.
+	 *
+	 * Non-core block files registered via block.json never use a '.min' suffix,
+	 * so storing a non-empty suffix causes str_replace() to search for '.min.css'
+	 * in a filename that only contains '.css', silently leaving the LTR URL
+	 * unchanged on RTL sites.
+	 *
+	 * @ticket 61625
+	 *
+	 * @covers ::register_block_style_handle
+	 */
+	public function test_register_block_style_handle_rtl_suffix_is_empty_for_non_core_blocks() {
+		global $wp_locale;
+
+		$metadata = array(
+			'file'  => DIR_TESTDATA . '/blocks/notice/block.json',
+			'name'  => 'tests/test-block-rtl-suffix',
+			'style' => 'file:./block.css',
+		);
+
+		$orig_text_dir             = $wp_locale->text_direction;
+		$wp_locale->text_direction = 'rtl';
+
+		register_block_style_handle( $metadata, 'style' );
+		$extra_suffix = wp_styles()->get_data( 'tests-test-block-rtl-suffix-style', 'suffix' );
+
+		$wp_locale->text_direction = $orig_text_dir;
+
+		$this->assertSame(
+			'',
+			$extra_suffix,
+			'Non-core block RTL styles must have an empty suffix so the LTR URL is correctly rewritten to the RTL URL, regardless of SCRIPT_DEBUG.'
+		);
+	}
+
 	/**
 	 * @ticket 56664
 	 */