diff --git a/packages/dependency-extraction-webpack-plugin/lib/index.js b/packages/dependency-extraction-webpack-plugin/lib/index.js
index cf780d7370dcf..8bc7cb2931216 100644
--- a/packages/dependency-extraction-webpack-plugin/lib/index.js
+++ b/packages/dependency-extraction-webpack-plugin/lib/index.js
@@ -387,6 +387,16 @@ class DependencyExtractionWebpackPlugin {
 				assetData.type = 'module';
 			}
 
+			if ( compilation.options?.optimization?.runtimeChunk !== false ) {
+				// Sets the script handle for the shared runtime file so WordPress registers it only once when using the asset file.
+				assetData.handle =
+					compilation.name +
+					'-' +
+					chunkJSFile
+						.replace( /\\/g, '/' )
+						.replace( jsExtensionRegExp, '' );
+			}
+
 			if ( combineAssets ) {
 				combinedAssetsData[ chunkJSFile ] = assetData;
 				continue;
diff --git a/packages/dependency-extraction-webpack-plugin/test/__snapshots__/build.js.snap b/packages/dependency-extraction-webpack-plugin/test/__snapshots__/build.js.snap
index 8ea40b00d7c2d..bafae8eb91486 100644
--- a/packages/dependency-extraction-webpack-plugin/test/__snapshots__/build.js.snap
+++ b/packages/dependency-extraction-webpack-plugin/test/__snapshots__/build.js.snap
@@ -265,17 +265,17 @@ exports[`DependencyExtractionWebpackPlugin modules Webpack \`polyfill-magic-comm
 exports[`DependencyExtractionWebpackPlugin modules Webpack \`polyfill-magic-comment-minified\` should produce expected output: External modules should match snapshot 1`] = `[]`;
 
 exports[`DependencyExtractionWebpackPlugin modules Webpack \`runtime-chunk-single\` should produce expected output: Asset file 'a.asset.php' should match snapshot 1`] = `
-"<?php return array('dependencies' => array('@wordpress/blob'), 'version' => 'ee5ac21a1f0003d732e6', 'type' => 'module');
+"<?php return array('dependencies' => array('@wordpress/blob'), 'version' => 'ee5ac21a1f0003d732e6', 'type' => 'module', 'handle' => 'runtime-chunk-single-modules-a');
 "
 `;
 
 exports[`DependencyExtractionWebpackPlugin modules Webpack \`runtime-chunk-single\` should produce expected output: Asset file 'b.asset.php' should match snapshot 1`] = `
-"<?php return array('dependencies' => array('@wordpress/blob', 'lodash'), 'version' => '5b112b32c6db548c2997', 'type' => 'module');
+"<?php return array('dependencies' => array('@wordpress/blob', 'lodash'), 'version' => '5b112b32c6db548c2997', 'type' => 'module', 'handle' => 'runtime-chunk-single-modules-b');
 "
 `;
 
 exports[`DependencyExtractionWebpackPlugin modules Webpack \`runtime-chunk-single\` should produce expected output: Asset file 'runtime.asset.php' should match snapshot 1`] = `
-"<?php return array('dependencies' => array(), 'version' => 'b1ca4106075e0bd94f9c', 'type' => 'module');
+"<?php return array('dependencies' => array(), 'version' => 'b1ca4106075e0bd94f9c', 'type' => 'module', 'handle' => 'runtime-chunk-single-modules-runtime');
 "
 `;
 
@@ -681,17 +681,17 @@ exports[`DependencyExtractionWebpackPlugin scripts Webpack \`polyfill-magic-comm
 exports[`DependencyExtractionWebpackPlugin scripts Webpack \`polyfill-magic-comment-minified\` should produce expected output: External modules should match snapshot 1`] = `[]`;
 
 exports[`DependencyExtractionWebpackPlugin scripts Webpack \`runtime-chunk-single\` should produce expected output: Asset file 'a.asset.php' should match snapshot 1`] = `
-"<?php return array('dependencies' => array('wp-blob'), 'version' => 'd091f1cbbf7603d6e12c');
+"<?php return array('dependencies' => array('wp-blob'), 'version' => 'd091f1cbbf7603d6e12c', 'handle' => 'runtime-chunk-single-scripts-a');
 "
 `;
 
 exports[`DependencyExtractionWebpackPlugin scripts Webpack \`runtime-chunk-single\` should produce expected output: Asset file 'b.asset.php' should match snapshot 1`] = `
-"<?php return array('dependencies' => array('lodash', 'wp-blob'), 'version' => '845bc6d4ffbdb9419ebd');
+"<?php return array('dependencies' => array('lodash', 'wp-blob'), 'version' => '845bc6d4ffbdb9419ebd', 'handle' => 'runtime-chunk-single-scripts-b');
 "
 `;
 
 exports[`DependencyExtractionWebpackPlugin scripts Webpack \`runtime-chunk-single\` should produce expected output: Asset file 'runtime.asset.php' should match snapshot 1`] = `
-"<?php return array('dependencies' => array(), 'version' => '717eb779e609d175a7dd');
+"<?php return array('dependencies' => array(), 'version' => '717eb779e609d175a7dd', 'handle' => 'runtime-chunk-single-scripts-runtime');
 "
 `;
 
diff --git a/packages/scripts/CHANGELOG.md b/packages/scripts/CHANGELOG.md
index 55143ae792ae5..ceaa25c4ff9a0 100644
--- a/packages/scripts/CHANGELOG.md
+++ b/packages/scripts/CHANGELOG.md
@@ -2,6 +2,10 @@
 
 ## Unreleased
 
+### Bug Fix
+
+-   Make React Fast Refresh in the `start` command work with multiple blocks ([64924](https://github.com/WordPress/gutenberg/pull/64924)).
+
 ## 30.6.0 (2024-11-27)
 
 ## 30.5.1 (2024-11-18)
diff --git a/packages/scripts/config/webpack.config.js b/packages/scripts/config/webpack.config.js
index f9ef7dc5b7acc..2c3d423fcbd1e 100644
--- a/packages/scripts/config/webpack.config.js
+++ b/packages/scripts/config/webpack.config.js
@@ -7,7 +7,7 @@ const CopyWebpackPlugin = require( 'copy-webpack-plugin' );
 const webpack = require( 'webpack' );
 const browserslist = require( 'browserslist' );
 const MiniCSSExtractPlugin = require( 'mini-css-extract-plugin' );
-const { basename, dirname, resolve } = require( 'path' );
+const { basename, dirname, relative, resolve, sep } = require( 'path' );
 const ReactRefreshWebpackPlugin = require( '@pmmmwh/react-refresh-webpack-plugin' );
 const RtlCssPlugin = require( 'rtlcss-webpack-plugin' );
 const TerserPlugin = require( 'terser-webpack-plugin' );
@@ -115,6 +115,7 @@ const baseConfig = {
 	optimization: {
 		// Only concatenate modules in production, when not analyzing bundles.
 		concatenateModules: isProduction && ! process.env.WP_BUNDLE_ANALYZER,
+		runtimeChunk: hasReactFastRefresh && 'single',
 		splitChunks: {
 			cacheGroups: {
 				style: {
@@ -340,6 +341,32 @@ const scriptConfig = {
 								}
 							} );
 
+							if ( hasReactFastRefresh ) {
+								// Prepends the file reference to the shared runtime chunk to every script type defined for the block.
+								const runtimePath = relative(
+									dirname( absoluteFrom ),
+									fromProjectRoot(
+										getWordPressSrcDirectory() +
+											sep +
+											'runtime.js'
+									)
+								);
+								const fields =
+									getBlockJsonScriptFields( blockJson );
+								for ( const [ fieldName ] of Object.entries(
+									fields
+								) ) {
+									blockJson[ fieldName ] = [
+										`file:${ runtimePath }`,
+										...( Array.isArray(
+											blockJson[ fieldName ]
+										)
+											? blockJson[ fieldName ]
+											: [ blockJson[ fieldName ] ] ),
+									];
+								}
+							}
+
 							return JSON.stringify( blockJson, null, 2 );
 						}