diff --git a/.changeset/empty-hats-own.md b/.changeset/empty-hats-own.md
new file mode 100644
index 0000000000..21d80658bc
--- /dev/null
+++ b/.changeset/empty-hats-own.md
@@ -0,0 +1,5 @@
+---
+'@shopify/theme': patch
+---
+
+Fix hot reloading of `.css.liquid` and `.js.liquid` assets.
diff --git a/packages/theme/src/cli/utilities/theme-environment/hot-reload/client.ts b/packages/theme/src/cli/utilities/theme-environment/hot-reload/client.ts
index cb43df4d28..4f6e23f5b5 100644
--- a/packages/theme/src/cli/utilities/theme-environment/hot-reload/client.ts
+++ b/packages/theme/src/cli/utilities/theme-environment/hot-reload/client.ts
@@ -64,9 +64,13 @@ function hotReloadScript() {
 
   const refreshHTMLLinkElements = (elements: HTMLLinkElement[]) => {
     for (const element of elements) {
-      // The `href` property prepends the host to the pathname. Use attributes instead:
-      // eslint-disable-next-line @typescript-eslint/no-non-null-assertion
-      element.setAttribute('href', element.getAttribute('href')!.replace(/v=\d+$/, `v=${Date.now()}`))
+      // The `href` property prepends the host to the pathname. Use attributes instead.
+      // Note: when a .liquid asset is requested but not found in SFR, it will be rendered as
+      // `.../assets/file.css?1234` instead of `.../assets/file.css?v=1234`. Ensure we target both.
+      element.setAttribute(
+        'href',
+        (element.getAttribute('href') ?? '').replace(/(\?|&)(?:v=)?\d+$/, `$1v=${Date.now()}`),
+      )
     }
   }
 
diff --git a/packages/theme/src/cli/utilities/theme-environment/hot-reload/server.test.ts b/packages/theme/src/cli/utilities/theme-environment/hot-reload/server.test.ts
index 0d8283eaf8..be4d29057d 100644
--- a/packages/theme/src/cli/utilities/theme-environment/hot-reload/server.test.ts
+++ b/packages/theme/src/cli/utilities/theme-environment/hot-reload/server.test.ts
@@ -178,7 +178,8 @@ describe('hot-reload server', () => {
     // Emits a CSS HotReload event after syncing:
     expect(cssLiquidSyncSpy).toHaveBeenCalled()
     await nextTick()
-    expect(hotReloadEvents.at(-1)).toMatch(`data: {"type":"full","key":"${cssLiquidFileKey}"}`)
+    // Removes the `.liquid` extension before sending it to the browser:
+    expect(hotReloadEvents.at(-1)).toMatch(`data: {"type":"css","key":"${cssLiquidFileKey.replace('.liquid', '')}"}`)
 
     // -- Updates other files:
     const jsFileKey = 'assets/something.js'
diff --git a/packages/theme/src/cli/utilities/theme-environment/hot-reload/server.ts b/packages/theme/src/cli/utilities/theme-environment/hot-reload/server.ts
index a281d96355..2bce016ae2 100644
--- a/packages/theme/src/cli/utilities/theme-environment/hot-reload/server.ts
+++ b/packages/theme/src/cli/utilities/theme-environment/hot-reload/server.ts
@@ -97,7 +97,7 @@ export function setupInMemoryTemplateWatcher(ctx: DevServerContext) {
     if (isAsset(fileKey)) {
       if (extension === '.liquid') {
         // If the asset is a .css.liquid or similar, we wait until it's been synced:
-        onSync(() => triggerHotReload(fileKey, ctx))
+        onSync(() => triggerHotReload(fileKey.replace(extension, ''), ctx))
       } else {
         // Otherwise, just full refresh directly:
         triggerHotReload(fileKey, ctx)
diff --git a/packages/theme/src/cli/utilities/theme-environment/proxy.ts b/packages/theme/src/cli/utilities/theme-environment/proxy.ts
index 61a70a68a3..fb3246ca51 100644
--- a/packages/theme/src/cli/utilities/theme-environment/proxy.ts
+++ b/packages/theme/src/cli/utilities/theme-environment/proxy.ts
@@ -235,6 +235,15 @@ function proxyStorefrontRequest(event: H3Event, ctx: DevServerContext) {
   const path = event.path.replaceAll(EXTENSION_CDN_PREFIX, '/')
   const host = event.path.startsWith(EXTENSION_CDN_PREFIX) ? 'cdn.shopify.com' : ctx.session.storeFqdn
   const url = new URL(path, `https://${host}`)
+
+  // When a .css.liquid or .js.liquid file is requested but it doesn't exist in SFR,
+  // it will be rendered with a query string like `assets/file.css?1234`.
+  // For some reason, after refreshing, this rendered URL keeps the wrong `?1234`
+  // query string for a while. We replace it with a proper timestamp here to fix it.
+  if (/\/assets\/[^/]+\.(css|js)$/.test(url.pathname) && /\?\d+$/.test(url.search)) {
+    url.search = `?v=${Date.now()}`
+  }
+
   url.searchParams.set('_fd', '0')
   url.searchParams.set('pb', '0')
   const headers = getProxyStorefrontHeaders(event)
diff --git a/packages/theme/src/cli/utilities/theme-environment/theme-environment.test.ts b/packages/theme/src/cli/utilities/theme-environment/theme-environment.test.ts
index b8a9dc86fb..c07ef0c624 100644
--- a/packages/theme/src/cli/utilities/theme-environment/theme-environment.test.ts
+++ b/packages/theme/src/cli/utilities/theme-environment/theme-environment.test.ts
@@ -347,5 +347,22 @@ describe('setupDevServer', () => {
       const {body} = await eventPromise
       expect(body).toMatch(`src: url(/cdn/shop/t/img/assets/font.woff2)`)
     })
+
+    test('proxies .js.liquid assets replacing the error query string', async () => {
+      const fetchStub = vi.fn(() => new Response())
+      vi.stubGlobal('fetch', fetchStub)
+      vi.useFakeTimers()
+      const now = Date.now()
+
+      const pathname = '/cdn/shop/t/img/assets/file4.js'
+      const eventPromise = dispatchEvent(`${pathname}?1234`)
+      await expect(eventPromise).resolves.not.toThrow()
+      expect(vi.mocked(render)).not.toHaveBeenCalled()
+
+      expect(fetchStub).toHaveBeenCalledWith(
+        `https://${defaultServerContext.session.storeFqdn}${pathname}?v=${now}&_fd=0&pb=0`,
+        expect.any(Object),
+      )
+    })
   })
 })