diff --git a/.changeset/bright-impalas-float.md b/.changeset/bright-impalas-float.md
new file mode 100644
index 00000000000..8dd3f4d3c17
--- /dev/null
+++ b/.changeset/bright-impalas-float.md
@@ -0,0 +1,5 @@
+---
+'@shopify/theme': minor
+---
+
+Render error overlay when `theme dev` encounters asset upload errors. A 500 status code is returned when the error overlay is rendered.
diff --git a/docs-shopify.dev/commands/interfaces/theme-dev.interface.ts b/docs-shopify.dev/commands/interfaces/theme-dev.interface.ts
index e8f131c9941..33bbbce0b4a 100644
--- a/docs-shopify.dev/commands/interfaces/theme-dev.interface.ts
+++ b/docs-shopify.dev/commands/interfaces/theme-dev.interface.ts
@@ -6,6 +6,15 @@ export interface themedev {
    */
   '-e, --environment <value>'?: string
 
+  /**
+   * Controls the visibility of the error overlay when an theme asset upload fails:
+- silent Prevents the error overlay from appearing.
+- default Displays the error overlay.
+      
+   * @environment SHOPIFY_FLAG_ERROR_OVERLAY
+   */
+  '--error-overlay <value>'?: string
+
   /**
    * Set which network interface the web server listens on. The default value is 127.0.0.1.
    * @environment SHOPIFY_FLAG_HOST
diff --git a/docs-shopify.dev/generated/generated_docs_data.json b/docs-shopify.dev/generated/generated_docs_data.json
index ace13faa9bc..c5156010559 100644
--- a/docs-shopify.dev/generated/generated_docs_data.json
+++ b/docs-shopify.dev/generated/generated_docs_data.json
@@ -4960,6 +4960,15 @@
             "name": "themedev",
             "description": "",
             "members": [
+              {
+                "filePath": "docs-shopify.dev/commands/interfaces/theme-dev.interface.ts",
+                "syntaxKind": "PropertySignature",
+                "name": "--error-overlay <value>",
+                "value": "string",
+                "description": "Controls the visibility of the error overlay when an theme asset upload fails: - silent Prevents the error overlay from appearing. - default Displays the error overlay.",
+                "isOptional": true,
+                "environmentValue": "SHOPIFY_FLAG_ERROR_OVERLAY"
+              },
               {
                 "filePath": "docs-shopify.dev/commands/interfaces/theme-dev.interface.ts",
                 "syntaxKind": "PropertySignature",
@@ -5114,7 +5123,7 @@
                 "environmentValue": "SHOPIFY_FLAG_IGNORE"
               }
             ],
-            "value": "export interface themedev {\n  /**\n   * The environment to apply to the current command.\n   * @environment SHOPIFY_FLAG_ENVIRONMENT\n   */\n  '-e, --environment <value>'?: string\n\n  /**\n   * Set which network interface the web server listens on. The default value is 127.0.0.1.\n   * @environment SHOPIFY_FLAG_HOST\n   */\n  '--host <value>'?: string\n\n  /**\n   * Skip hot reloading any files that match the specified pattern.\n   * @environment SHOPIFY_FLAG_IGNORE\n   */\n  '-x, --ignore <value>'?: string\n\n  /**\n   * The live reload mode switches the server behavior when a file is modified:\n- hot-reload Hot reloads local changes to CSS and sections (default)\n- full-page  Always refreshes the entire page\n- off        Deactivate live reload\n   * @environment SHOPIFY_FLAG_LIVE_RELOAD\n   */\n  '--live-reload <value>'?: string\n\n  /**\n   * Disable color output.\n   * @environment SHOPIFY_FLAG_NO_COLOR\n   */\n  '--no-color'?: ''\n\n  /**\n   * Prevents files from being deleted in the remote theme when a file has been deleted locally. This applies to files that are deleted while the command is running, and files that have been deleted locally before the command is run.\n   * @environment SHOPIFY_FLAG_NODELETE\n   */\n  '-n, --nodelete'?: ''\n\n  /**\n   * The file path or URL. The file path is to a file that you want updated on idle. The URL path is where you want a webhook posted to report on file changes.\n   * @environment SHOPIFY_FLAG_NOTIFY\n   */\n  '--notify <value>'?: string\n\n  /**\n   * Hot reload only files that match the specified pattern.\n   * @environment SHOPIFY_FLAG_ONLY\n   */\n  '-o, --only <value>'?: string\n\n  /**\n   * Automatically launch the theme preview in your default web browser.\n   * @environment SHOPIFY_FLAG_OPEN\n   */\n  '--open'?: ''\n\n  /**\n   * Password generated from the Theme Access app.\n   * @environment SHOPIFY_CLI_THEME_TOKEN\n   */\n  '--password <value>'?: string\n\n  /**\n   * The path to your theme directory.\n   * @environment SHOPIFY_FLAG_PATH\n   */\n  '--path <value>'?: string\n\n  /**\n   * Local port to serve theme preview from.\n   * @environment SHOPIFY_FLAG_PORT\n   */\n  '--port <value>'?: string\n\n  /**\n   * Store URL. It can be the store prefix (example) or the full myshopify.com URL (example.myshopify.com, https://example.myshopify.com).\n   * @environment SHOPIFY_FLAG_STORE\n   */\n  '-s, --store <value>'?: string\n\n  /**\n   * The password for storefronts with password protection.\n   * @environment SHOPIFY_FLAG_STORE_PASSWORD\n   */\n  '--store-password <value>'?: string\n\n  /**\n   * Theme ID or name of the remote theme.\n   * @environment SHOPIFY_FLAG_THEME_ID\n   */\n  '-t, --theme <value>'?: string\n\n  /**\n   * Synchronize Theme Editor updates in the local theme files.\n   * @environment SHOPIFY_FLAG_THEME_EDITOR_SYNC\n   */\n  '--theme-editor-sync'?: ''\n\n  /**\n   * Increase the verbosity of the output.\n   * @environment SHOPIFY_FLAG_VERBOSE\n   */\n  '--verbose'?: ''\n}"
+            "value": "export interface themedev {\n  /**\n   * The environment to apply to the current command.\n   * @environment SHOPIFY_FLAG_ENVIRONMENT\n   */\n  '-e, --environment <value>'?: string\n\n  /**\n   * Controls the visibility of the error overlay when an theme asset upload fails:\n- silent Prevents the error overlay from appearing.\n- default Displays the error overlay.\n      \n   * @environment SHOPIFY_FLAG_ERROR_OVERLAY\n   */\n  '--error-overlay <value>'?: string\n\n  /**\n   * Set which network interface the web server listens on. The default value is 127.0.0.1.\n   * @environment SHOPIFY_FLAG_HOST\n   */\n  '--host <value>'?: string\n\n  /**\n   * Skip hot reloading any files that match the specified pattern.\n   * @environment SHOPIFY_FLAG_IGNORE\n   */\n  '-x, --ignore <value>'?: string\n\n  /**\n   * The live reload mode switches the server behavior when a file is modified:\n- hot-reload Hot reloads local changes to CSS and sections (default)\n- full-page  Always refreshes the entire page\n- off        Deactivate live reload\n   * @environment SHOPIFY_FLAG_LIVE_RELOAD\n   */\n  '--live-reload <value>'?: string\n\n  /**\n   * Disable color output.\n   * @environment SHOPIFY_FLAG_NO_COLOR\n   */\n  '--no-color'?: ''\n\n  /**\n   * Prevents files from being deleted in the remote theme when a file has been deleted locally. This applies to files that are deleted while the command is running, and files that have been deleted locally before the command is run.\n   * @environment SHOPIFY_FLAG_NODELETE\n   */\n  '-n, --nodelete'?: ''\n\n  /**\n   * The file path or URL. The file path is to a file that you want updated on idle. The URL path is where you want a webhook posted to report on file changes.\n   * @environment SHOPIFY_FLAG_NOTIFY\n   */\n  '--notify <value>'?: string\n\n  /**\n   * Hot reload only files that match the specified pattern.\n   * @environment SHOPIFY_FLAG_ONLY\n   */\n  '-o, --only <value>'?: string\n\n  /**\n   * Automatically launch the theme preview in your default web browser.\n   * @environment SHOPIFY_FLAG_OPEN\n   */\n  '--open'?: ''\n\n  /**\n   * Password generated from the Theme Access app.\n   * @environment SHOPIFY_CLI_THEME_TOKEN\n   */\n  '--password <value>'?: string\n\n  /**\n   * The path to your theme directory.\n   * @environment SHOPIFY_FLAG_PATH\n   */\n  '--path <value>'?: string\n\n  /**\n   * Local port to serve theme preview from.\n   * @environment SHOPIFY_FLAG_PORT\n   */\n  '--port <value>'?: string\n\n  /**\n   * Store URL. It can be the store prefix (example) or the full myshopify.com URL (example.myshopify.com, https://example.myshopify.com).\n   * @environment SHOPIFY_FLAG_STORE\n   */\n  '-s, --store <value>'?: string\n\n  /**\n   * The password for storefronts with password protection.\n   * @environment SHOPIFY_FLAG_STORE_PASSWORD\n   */\n  '--store-password <value>'?: string\n\n  /**\n   * Theme ID or name of the remote theme.\n   * @environment SHOPIFY_FLAG_THEME_ID\n   */\n  '-t, --theme <value>'?: string\n\n  /**\n   * Synchronize Theme Editor updates in the local theme files.\n   * @environment SHOPIFY_FLAG_THEME_EDITOR_SYNC\n   */\n  '--theme-editor-sync'?: ''\n\n  /**\n   * Increase the verbosity of the output.\n   * @environment SHOPIFY_FLAG_VERBOSE\n   */\n  '--verbose'?: ''\n}"
           }
         }
       }
diff --git a/packages/cli/README.md b/packages/cli/README.md
index cf82abf4bd6..5d30082ac7b 100644
--- a/packages/cli/README.md
+++ b/packages/cli/README.md
@@ -1796,9 +1796,10 @@ Uploads the current theme as a development theme to the connected store, then pr
 
 ```
 USAGE
-  $ shopify theme dev [-e <value>] [--host <value>] [-x <value>] [--live-reload hot-reload|full-page|off]
-    [--no-color] [-n] [--notify <value>] [-o <value>] [--open] [--password <value>] [--path <value>] [--port <value>]
-    [-s <value>] [--store-password <value>] [-t <value>] [--theme-editor-sync] [--verbose]
+  $ shopify theme dev [-e <value>] [--error-overlay silent|default] [--host <value>] [-x <value>]
+    [--live-reload hot-reload|full-page|off] [--no-color] [-n] [--notify <value>] [-o <value>] [--open] [--password
+    <value>] [--path <value>] [--port <value>] [-s <value>] [--store-password <value>] [-t <value>]
+    [--theme-editor-sync] [--verbose]
 
 FLAGS
   -e, --environment=<value>
@@ -1821,6 +1822,13 @@ FLAGS
   -x, --ignore=<value>...
       Skip hot reloading any files that match the specified pattern.
 
+  --error-overlay=<option>
+      [default: default] Controls the visibility of the error overlay when an theme asset upload fails:
+      - silent Prevents the error overlay from appearing.
+      - default Displays the error overlay.
+
+      <options: silent|default>
+
   --host=<value>
       Set which network interface the web server listens on. The default value is 127.0.0.1.
 
diff --git a/packages/cli/oclif.manifest.json b/packages/cli/oclif.manifest.json
index 45ece7008d8..58f76eadbee 100644
--- a/packages/cli/oclif.manifest.json
+++ b/packages/cli/oclif.manifest.json
@@ -5123,6 +5123,19 @@
           "name": "environment",
           "type": "option"
         },
+        "error-overlay": {
+          "default": "default",
+          "description": "Controls the visibility of the error overlay when an theme asset upload fails:\n- silent Prevents the error overlay from appearing.\n- default Displays the error overlay.\n      ",
+          "env": "SHOPIFY_FLAG_ERROR_OVERLAY",
+          "hasDynamicHelp": false,
+          "multiple": false,
+          "name": "error-overlay",
+          "options": [
+            "silent",
+            "default"
+          ],
+          "type": "option"
+        },
         "force": {
           "allowNo": false,
           "char": "f",
@@ -6398,6 +6411,19 @@
           "name": "environment",
           "type": "option"
         },
+        "error-overlay": {
+          "default": "default",
+          "description": "Controls the visibility of the error overlay when an theme asset upload fails:\n- silent Prevents the error overlay from appearing.\n- default Displays the error overlay.\n      ",
+          "env": "SHOPIFY_FLAG_ERROR_OVERLAY",
+          "hasDynamicHelp": false,
+          "multiple": false,
+          "name": "error-overlay",
+          "options": [
+            "silent",
+            "default"
+          ],
+          "type": "option"
+        },
         "force": {
           "allowNo": false,
           "char": "f",
diff --git a/packages/theme/src/cli/commands/theme/dev.ts b/packages/theme/src/cli/commands/theme/dev.ts
index c0fedeaf24d..5979cbd4621 100644
--- a/packages/theme/src/cli/commands/theme/dev.ts
+++ b/packages/theme/src/cli/commands/theme/dev.ts
@@ -9,7 +9,7 @@ import {Flags} from '@oclif/core'
 import {globalFlags} from '@shopify/cli-kit/node/cli'
 import {Theme} from '@shopify/cli-kit/node/themes/types'
 import {ensureAuthenticatedThemes} from '@shopify/cli-kit/node/session'
-import type {LiveReload} from '../../utilities/theme-environment/types.js'
+import type {ErrorOverlayMode, LiveReload} from '../../utilities/theme-environment/types.js'
 
 export default class Dev extends ThemeCommand {
   static summary =
@@ -54,6 +54,15 @@ You can run this command only in a directory that matches the [default Shopify t
       options: ['hot-reload', 'full-page', 'off'],
       env: 'SHOPIFY_FLAG_LIVE_RELOAD',
     }),
+    'error-overlay': Flags.string({
+      description: `Controls the visibility of the error overlay when an theme asset upload fails:
+- silent Prevents the error overlay from appearing.
+- default Displays the error overlay.
+      `,
+      options: ['silent', 'default'],
+      default: 'default',
+      env: 'SHOPIFY_FLAG_ERROR_OVERLAY',
+    }),
     poll: Flags.boolean({
       hidden: true,
       description: 'Force polling to detect file changes.',
@@ -147,6 +156,7 @@ You can run this command only in a directory that matches the [default Shopify t
       host: flags.host,
       port: flags.port,
       'live-reload': flags['live-reload'] as LiveReload,
+      'error-overlay': flags['error-overlay'] as ErrorOverlayMode,
       force: flags.force,
       open: flags.open,
       'theme-editor-sync': flags['theme-editor-sync'],
diff --git a/packages/theme/src/cli/services/dev.test.ts b/packages/theme/src/cli/services/dev.test.ts
index 63d3ec8efee..b406997e8d1 100644
--- a/packages/theme/src/cli/services/dev.test.ts
+++ b/packages/theme/src/cli/services/dev.test.ts
@@ -50,6 +50,7 @@ describe('dev', () => {
     noDelete: false,
     ignore: [],
     only: [],
+    'error-overlay': 'default',
   }
 
   const session: DevServerSession = {
@@ -101,6 +102,7 @@ describe('dev', () => {
           ignore: [],
           noDelete: false,
           only: [],
+          errorOverlay: 'default',
         },
       })
     })
diff --git a/packages/theme/src/cli/services/dev.ts b/packages/theme/src/cli/services/dev.ts
index 93579799975..67c1fbd87f0 100644
--- a/packages/theme/src/cli/services/dev.ts
+++ b/packages/theme/src/cli/services/dev.ts
@@ -1,7 +1,7 @@
 import {hasRequiredThemeDirectories, mountThemeFileSystem} from '../utilities/theme-fs.js'
 import {ensureDirectoryConfirmed} from '../utilities/theme-ui.js'
 import {setupDevServer} from '../utilities/theme-environment/theme-environment.js'
-import {DevServerContext, LiveReload} from '../utilities/theme-environment/types.js'
+import {DevServerContext, ErrorOverlayMode, LiveReload} from '../utilities/theme-environment/types.js'
 import {isStorefrontPasswordProtected} from '../utilities/theme-environment/storefront-session.js'
 import {ensureValidPassword} from '../utilities/theme-environment/storefront-password-prompt.js'
 import {emptyThemeExtFileSystem} from '../utilities/theme-fs-empty.js'
@@ -31,6 +31,7 @@ export interface DevOptions {
   force: boolean
   'theme-editor-sync': boolean
   'live-reload': LiveReload
+  'error-overlay': ErrorOverlayMode
   noDelete: boolean
   ignore: string[]
   only: string[]
@@ -90,6 +91,7 @@ export async function dev(options: DevOptions) {
       noDelete: options.noDelete,
       ignore: options.ignore,
       only: options.only,
+      errorOverlay: options['error-overlay'],
     },
   }
 
diff --git a/packages/theme/src/cli/utilities/theme-environment/hot-reload/error-page.ts b/packages/theme/src/cli/utilities/theme-environment/hot-reload/error-page.ts
new file mode 100644
index 00000000000..e81f09c5741
--- /dev/null
+++ b/packages/theme/src/cli/utilities/theme-environment/hot-reload/error-page.ts
@@ -0,0 +1,92 @@
+interface Error {
+  message: string
+  code: string
+}
+
+const POLARIS_STYLESHEET_URL = 'https://unpkg.com/@shopify/polaris@13.9.2/build/esm/styles.css'
+
+function escapeHtml(unsafe: string) {
+  return unsafe
+    .replace(/&/g, '&amp;')
+    .replace(/</g, '&lt;')
+    .replace(/>/g, '&gt;')
+    .replace(/"/g, '&quot;')
+    .replace(/'/g, '&#039;')
+}
+
+export function getErrorPage(options: {title: string; header: string; errors: Error[]}) {
+  const html = String.raw
+  return html`<!DOCTYPE html>
+    <html>
+      <head>
+        <title>${options.title ?? 'Upload Errors'}</title>
+        <link rel="stylesheet" href="${POLARIS_STYLESHEET_URL}" />
+      </head>
+      <body>
+        <div style="display: flex; justify-content: center; padding-top: 2rem;">
+          <div style="width: 80%;">
+            <div class="Polaris-Banner Polaris-Banner--withinPage" tabindex="0" role="alert" aria-live="polite">
+              <div class="Polaris-Box" style="--pc-box-width:100%">
+                <div
+                  class="Polaris-BlockStack"
+                  style="--pc-block-stack-align:space-between;--pc-block-stack-order:column"
+                >
+                  <div
+                    class="Polaris-Box"
+                    style="--pc-box-color: var(--p-color-text-critical-on-bg-fill); --pc-box-background: var(--p-color-bg-fill-critical); --pc-box-padding-block-start-xs: var(--p-space-300); --pc-box-padding-block-end-xs: var(--p-space-300); --pc-box-padding-inline-start-xs: var(--p-space-300); --pc-box-padding-inline-end-xs: var(--p-space-300); --pc-box-border-start-start-radius: var(--p-border-radius-300); --pc-box-border-start-end-radius: var(--p-border-radius-300);"
+                  >
+                    <div
+                      class="Polaris-InlineStack"
+                      style="--pc-inline-stack-align:space-between;--pc-inline-stack-block-align:center;--pc-inline-stack-wrap:nowrap;--pc-inline-stack-gap-xs:var(--p-space-200);--pc-inline-stack-flex-direction-xs:row"
+                    >
+                      <div
+                        class="Polaris-InlineStack"
+                        style="--pc-inline-stack-wrap:nowrap;--pc-inline-stack-gap-xs:var(--p-space-100);--pc-inline-stack-flex-direction-xs:row"
+                      >
+                        <span class="Polaris-Banner--textCriticalOnBgFill">
+                          <span class="Polaris-Icon">
+                            <svg xmlns="http://www.w3.org/2000/svg" viewBox="0 0 20 20">
+                              <path d="M10 6a.75.75 0 0 1 .75.75v3.5a.75.75 0 0 1-1.5 0v-3.5a.75.75 0 0 1 .75-.75Z" />
+                              <path d="M11 13a1 1 0 1 1-2 0 1 1 0 0 1 2 0Z" />
+                              <path
+                                fill-rule="evenodd"
+                                d="M17 10a7 7 0 1 1-14 0 7 7 0 0 1 14 0Zm-1.5 0a5.5 5.5 0 1 1-11 0 5.5 5.5 0 0 1 11 0Z"
+                              />
+                            </svg>
+                          </span>
+                        </span>
+                        <h2 class="Polaris-Text--root Polaris-Text--headingSm Polaris-Text--break">
+                          ${options.header}
+                        </h2>
+                      </div>
+                    </div>
+                  </div>
+                  <div
+                    class="Polaris-Box"
+                    style="--pc-box-padding-block-start-xs:var(--p-space-300);--pc-box-padding-block-end-xs:var(--p-space-300);--pc-box-padding-block-end-md:var(--p-space-400);--pc-box-padding-inline-start-xs:var(--p-space-300);--pc-box-padding-inline-start-md:var(--p-space-400);--pc-box-padding-inline-end-xs:var(--p-space-300);--pc-box-padding-inline-end-md:var(--p-space-400)"
+                  >
+                    <div
+                      class="Polaris-BlockStack"
+                      style="--pc-block-stack-order:column;--pc-block-stack-gap-xs:var(--p-space-300)"
+                    >
+                      ${options.errors
+                        .map(
+                          (error) => `
+                          <div>
+                            <span class="Polaris-Text--root Polaris-Text--headingSm">${escapeHtml(error.message)}</span>
+                            <ul class="Polaris-List">
+                              <li class="Polaris-List__Item">${escapeHtml(error.code)}</li>
+                            </ul>
+                          </div>`,
+                        )
+                        .join('')}
+                    </div>
+                  </div>
+                </div>
+              </div>
+            </div>
+          </div>
+        </div>
+      </body>
+    </html>`
+}
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 6c66b4b745b..58ec32bafb6 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
@@ -330,6 +330,7 @@ function createTestContext(options?: {files?: [string, string][]}) {
       liveReload: 'hot-reload',
       open: false,
       themeEditorSync: false,
+      errorOverlay: 'default',
     },
   }
 
diff --git a/packages/theme/src/cli/utilities/theme-environment/html.ts b/packages/theme/src/cli/utilities/theme-environment/html.ts
index 8e6097da653..f24493978a2 100644
--- a/packages/theme/src/cli/utilities/theme-environment/html.ts
+++ b/packages/theme/src/cli/utilities/theme-environment/html.ts
@@ -1,9 +1,10 @@
 import {getProxyStorefrontHeaders, patchRenderingResponse} from './proxy.js'
 import {getInMemoryTemplates, injectHotReloadScript} from './hot-reload/server.js'
 import {render} from './storefront-renderer.js'
+import {getErrorPage} from './hot-reload/error-page.js'
 import {getExtensionInMemoryTemplates} from '../theme-ext-environment/theme-ext-server.js'
 import {logRequestLine} from '../log-request-line.js'
-import {defineEventHandler, getCookie, setResponseHeader, setResponseStatus, type H3Error} from 'h3'
+import {defineEventHandler, getCookie, H3Event, setResponseHeader, setResponseStatus, type H3Error} from 'h3'
 import {renderError, renderFatalError} from '@shopify/cli-kit/node/ui'
 import {AbortError} from '@shopify/cli-kit/node/error'
 import type {Response} from '@shopify/cli-kit/node/http'
@@ -14,6 +15,13 @@ export function getHtmlHandler(theme: Theme, ctx: DevServerContext) {
   return defineEventHandler((event) => {
     const [browserPathname = '/', browserSearch = ''] = event.path.split('?')
 
+    const shouldRenderUploadErrorPage =
+      ctx.options.errorOverlay !== 'silent' && ctx.localThemeFileSystem.uploadErrors.size > 0
+
+    if (shouldRenderUploadErrorPage) {
+      return renderUploadErrorPage(ctx, event)
+    }
+
     return render(ctx.session, {
       method: event.method,
       path: browserPathname,
@@ -52,8 +60,12 @@ export function getHtmlHandler(theme: Theme, ctx: DevServerContext) {
         let errorPageHtml = getErrorPage({
           title,
           header: title,
-          message: [...rest, cause?.message ?? error.message].join('<br>'),
-          code: error.stack?.replace(`${error.message}\n`, '') ?? '',
+          errors: [
+            {
+              message: [...rest, cause?.message ?? error.message].join('<br>'),
+              code: error.stack?.replace(`${error.message}\n`, '') ?? '',
+            },
+          ],
         })
 
         if (ctx.options.liveReload !== 'off') {
@@ -65,22 +77,23 @@ export function getHtmlHandler(theme: Theme, ctx: DevServerContext) {
   })
 }
 
-function getErrorPage(options: {title: string; header: string; message: string; code: string}) {
-  const html = String.raw
-
-  return html`<html>
-    <head>
-      <title>${options.title ?? 'Unknown error'}</title>
-    </head>
-    <body
-      id="full-error-page"
-      style="display: flex; flex-direction: column; align-items: center; padding-top: 20px; font-family: Arial"
-    >
-      <h2>${options.header}</h2>
-      <p>${options.message}</p>
-      <pre>${options.code}</pre>
-    </body>
-  </html>`
+function renderUploadErrorPage(ctx: DevServerContext, event: H3Event) {
+  setResponseStatus(event, 500, 'Failed to Upload Theme Files')
+  setResponseHeader(event, 'Content-Type', 'text/html')
+  let html = getErrorPage({
+    title: 'Failed to Upload Theme Files',
+    header: 'Upload Errors',
+    errors: Array.from(ctx.localThemeFileSystem.uploadErrors.entries()).map(([file, errors]) => ({
+      message: file,
+      code: errors.join('\n'),
+    })),
+  })
+
+  if (ctx.options.liveReload !== 'off') {
+    html = injectHotReloadScript(html)
+  }
+
+  return html
 }
 
 function assertThemeId(response: Response, html: string, expectedThemeId: string) {
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 355665ccf1f..867ac2aab3f 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
@@ -96,6 +96,7 @@ describe('setupDevServer', () => {
       liveReload: 'hot-reload',
       open: false,
       themeEditorSync: false,
+      errorOverlay: 'default',
     },
   }
 
diff --git a/packages/theme/src/cli/utilities/theme-environment/types.ts b/packages/theme/src/cli/utilities/theme-environment/types.ts
index cff737cd350..3dee51c7137 100644
--- a/packages/theme/src/cli/utilities/theme-environment/types.ts
+++ b/packages/theme/src/cli/utilities/theme-environment/types.ts
@@ -49,6 +49,13 @@ export interface DevServerSession extends AdminSession {
  */
 export type LiveReload = 'hot-reload' | 'full-page' | 'off'
 
+/**
+ * Controls the visibility of the error overlay when an asset upload fails. Options: ['silent', 'default']
+ * - silent: Prevents the error overlay from appearing.
+ * - default: Displays the error overlay.
+ */
+export type ErrorOverlayMode = 'silent' | 'default'
+
 /**
  * Maintains the state of local and remote assets in theme development server.
  */
@@ -117,6 +124,11 @@ export interface DevServerContext {
      * Automatically open the theme preview in the default browser.
      */
     open: boolean
+
+    /**
+     * Controls the visibility of the error overlay when an asset upload fails.
+     */
+    errorOverlay: ErrorOverlayMode
   }
 }
 
diff --git a/packages/theme/src/cli/utilities/theme-ext-environment/theme-ext-server.ts b/packages/theme/src/cli/utilities/theme-ext-environment/theme-ext-server.ts
index 4dea217cf48..c8f76e6465d 100644
--- a/packages/theme/src/cli/utilities/theme-ext-environment/theme-ext-server.ts
+++ b/packages/theme/src/cli/utilities/theme-ext-environment/theme-ext-server.ts
@@ -90,6 +90,7 @@ async function contextDevServerContext(
       port: port.toString(),
       liveReload: 'hot-reload',
       open: false,
+      errorOverlay: 'default',
     },
   }
 }
diff --git a/packages/theme/src/cli/utilities/theme-fs.ts b/packages/theme/src/cli/utilities/theme-fs.ts
index 1f8d997738c..a27a1b5e4b4 100644
--- a/packages/theme/src/cli/utilities/theme-fs.ts
+++ b/packages/theme/src/cli/utilities/theme-fs.ts
@@ -2,6 +2,7 @@ import {calculateChecksum} from './asset-checksum.js'
 import {applyIgnoreFilters, getPatternsFromShopifyIgnore} from './asset-ignore.js'
 import {Notifier} from './notifier.js'
 import {createSyncingCatchError} from './errors.js'
+import {emitHotReloadEvent} from './theme-environment/hot-reload/server.js'
 import {DEFAULT_IGNORE_PATTERNS, timestampDateFormat} from '../constants.js'
 import {glob, readFile, ReadOptions, fileExists, mkdir, writeFile, removeFile} from '@shopify/cli-kit/node/fs'
 import {joinPath, basename, relativePath} from '@shopify/cli-kit/node/path'
@@ -150,9 +151,11 @@ export function mountThemeFileSystem(root: string, options?: ThemeFileSystemOpti
 
         if (result?.success) {
           uploadErrors.delete(fileKey)
+          emitHotReloadEvent({type: 'full', key: fileKey})
         } else {
           const errors = result?.errors?.asset ?? ['Response was not successful.']
           uploadErrors.set(fileKey, errors)
+          emitHotReloadEvent({type: 'full', key: fileKey})
           throw new Error(errors.join('\n'))
         }
 
diff --git a/packages/theme/src/cli/utilities/theme-uploader.ts b/packages/theme/src/cli/utilities/theme-uploader.ts
index f07405a9067..c79301a5eee 100644
--- a/packages/theme/src/cli/utilities/theme-uploader.ts
+++ b/packages/theme/src/cli/utilities/theme-uploader.ts
@@ -2,6 +2,7 @@ import {partitionThemeFiles} from './theme-fs.js'
 import {rejectGeneratedStaticAssets} from './asset-checksum.js'
 import {renderTasksToStdErr} from './theme-ui.js'
 import {createSyncingCatchError, renderThrownError} from './errors.js'
+import {emitHotReloadEvent} from './theme-environment/hot-reload/server.js'
 import {AdminSession} from '@shopify/cli-kit/node/session'
 import {Result, Checksum, Theme, ThemeFileSystem} from '@shopify/cli-kit/node/themes/types'
 import {AssetParams, bulkUploadThemeAssets, deleteThemeAssets} from '@shopify/cli-kit/node/themes/api'
@@ -392,6 +393,7 @@ export function updateUploadErrors(result: Result, localThemeFileSystem: ThemeFi
   } else {
     const errors = result.errors?.asset ?? ['Response was not successful.']
     localThemeFileSystem.uploadErrors.set(result.key, errors)
+    emitHotReloadEvent({type: 'full', key: result.key})
   }
 }