diff --git a/packages/react-dev-overlay/src/internal/components/LeftRightDialogHeader/LeftRightDialogHeader.tsx b/packages/react-dev-overlay/src/internal/components/LeftRightDialogHeader/LeftRightDialogHeader.tsx
index e7e3167d0b1ca..cb8b722894484 100644
--- a/packages/react-dev-overlay/src/internal/components/LeftRightDialogHeader/LeftRightDialogHeader.tsx
+++ b/packages/react-dev-overlay/src/internal/components/LeftRightDialogHeader/LeftRightDialogHeader.tsx
@@ -1,4 +1,5 @@
 import * as React from 'react'
+import { CloseIcon } from '../../icons/CloseIcon'
 
 export type LeftRightDialogHeaderProps = {
   className?: string
@@ -147,34 +148,14 @@ const LeftRightDialogHeader: React.FC<LeftRightDialogHeaderProps> =
         </nav>
         {close ? (
           <button
+            data-nextjs-errors-dialog-left-right-close-button
             ref={buttonClose}
             type="button"
             onClick={close}
             aria-label="Close"
           >
             <span aria-hidden="true">
-              <svg
-                width="24"
-                height="24"
-                viewBox="0 0 24 24"
-                fill="none"
-                xmlns="http://www.w3.org/2000/svg"
-              >
-                <path
-                  d="M18 6L6 18"
-                  stroke="currentColor"
-                  strokeWidth="2"
-                  strokeLinecap="round"
-                  strokeLinejoin="round"
-                />
-                <path
-                  d="M6 6L18 18"
-                  stroke="currentColor"
-                  strokeWidth="2"
-                  strokeLinecap="round"
-                  strokeLinejoin="round"
-                />
-              </svg>
+              <CloseIcon />
             </span>
           </button>
         ) : null}
diff --git a/packages/react-dev-overlay/src/internal/container/Errors.tsx b/packages/react-dev-overlay/src/internal/container/Errors.tsx
index 556d3bd29d994..bead04084b3dd 100644
--- a/packages/react-dev-overlay/src/internal/container/Errors.tsx
+++ b/packages/react-dev-overlay/src/internal/container/Errors.tsx
@@ -17,6 +17,7 @@ import { Toast } from '../components/Toast'
 import { getErrorByType, ReadyRuntimeError } from '../helpers/getErrorByType'
 import { isNodeError } from '../helpers/nodeStackFrames'
 import { noop as css } from '../helpers/noop-template'
+import { CloseIcon } from '../icons/CloseIcon'
 import { RuntimeError } from './RuntimeError'
 
 export type SupportedErrorEvent = {
@@ -136,7 +137,9 @@ export const Errors: React.FC<ErrorsProps> = function Errors({ errors }) {
     }
   }, [nextError])
 
-  const [isMinimized, setMinimized] = React.useState<boolean>(false)
+  const [displayState, setDisplayState] = React.useState<
+    'minimized' | 'fullscreen' | 'hidden'
+  >('fullscreen')
   const [activeIdx, setActiveIndex] = React.useState<number>(0)
   const previous = React.useCallback((e?: MouseEvent | TouchEvent) => {
     e?.preventDefault()
@@ -162,19 +165,23 @@ export const Errors: React.FC<ErrorsProps> = function Errors({ errors }) {
   React.useEffect(() => {
     if (errors.length < 1) {
       setLookups({})
-      setMinimized(false)
+      setDisplayState('hidden')
       setActiveIndex(0)
     }
   }, [errors.length])
 
   const minimize = React.useCallback((e?: MouseEvent | TouchEvent) => {
     e?.preventDefault()
-    setMinimized(true)
+    setDisplayState('minimized')
   }, [])
-  const reopen = React.useCallback(
+  const hide = React.useCallback((e?: MouseEvent | TouchEvent) => {
+    e?.preventDefault()
+    setDisplayState('hidden')
+  }, [])
+  const fullscreen = React.useCallback(
     (e?: React.MouseEvent<HTMLDivElement, MouseEvent>) => {
       e?.preventDefault()
-      setMinimized(false)
+      setDisplayState('fullscreen')
     },
     []
   )
@@ -190,9 +197,13 @@ export const Errors: React.FC<ErrorsProps> = function Errors({ errors }) {
     return <Overlay />
   }
 
-  if (isMinimized) {
+  if (displayState === 'hidden') {
+    return null
+  }
+
+  if (displayState === 'minimized') {
     return (
-      <Toast className="nextjs-toast-errors-parent" onClick={reopen}>
+      <Toast className="nextjs-toast-errors-parent" onClick={fullscreen}>
         <div className="nextjs-toast-errors">
           <svg
             xmlns="http://www.w3.org/2000/svg"
@@ -212,6 +223,18 @@ export const Errors: React.FC<ErrorsProps> = function Errors({ errors }) {
           <span>
             {readyErrors.length} error{readyErrors.length > 1 ? 's' : ''}
           </span>
+          <button
+            data-nextjs-toast-errors-hide-button
+            className="nextjs-toast-errors-hide-button"
+            type="button"
+            onClick={(e) => {
+              e.stopPropagation()
+              hide()
+            }}
+            aria-label="Hide Errors"
+          >
+            <CloseIcon />
+          </button>
         </div>
       </Toast>
     )
@@ -320,4 +343,16 @@ export const styles = css`
   .nextjs-toast-errors > svg {
     margin-right: var(--size-gap);
   }
+  .nextjs-toast-errors-hide-button {
+    margin-left: var(--size-gap-triple);
+    border: none;
+    background: none;
+    color: var(--color-ansi-bright-white);
+    padding: 0;
+    transition: opacity 0.25s ease;
+    opacity: 0.7;
+  }
+  .nextjs-toast-errors-hide-button:hover {
+    opacity: 1;
+  }
 `
diff --git a/packages/react-dev-overlay/src/internal/icons/CloseIcon.tsx b/packages/react-dev-overlay/src/internal/icons/CloseIcon.tsx
new file mode 100644
index 0000000000000..e5a51a44a3eb5
--- /dev/null
+++ b/packages/react-dev-overlay/src/internal/icons/CloseIcon.tsx
@@ -0,0 +1,30 @@
+import * as React from 'react'
+
+const CloseIcon = () => {
+  return (
+    <svg
+      width="24"
+      height="24"
+      viewBox="0 0 24 24"
+      fill="none"
+      xmlns="http://www.w3.org/2000/svg"
+    >
+      <path
+        d="M18 6L6 18"
+        stroke="currentColor"
+        strokeWidth="2"
+        strokeLinecap="round"
+        strokeLinejoin="round"
+      />
+      <path
+        d="M6 6L18 18"
+        stroke="currentColor"
+        strokeWidth="2"
+        strokeLinecap="round"
+        strokeLinejoin="round"
+      />
+    </svg>
+  )
+}
+
+export { CloseIcon }
diff --git a/packages/react-dev-overlay/src/internal/styles/Base.tsx b/packages/react-dev-overlay/src/internal/styles/Base.tsx
index 0cc24069348fa..b48e0a25b2f9a 100644
--- a/packages/react-dev-overlay/src/internal/styles/Base.tsx
+++ b/packages/react-dev-overlay/src/internal/styles/Base.tsx
@@ -9,6 +9,7 @@ export function Base() {
           --size-gap-half: 4px;
           --size-gap: 8px;
           --size-gap-double: 16px;
+          --size-gap-triple: 24px;
           --size-gap-quad: 32px;
 
           --size-font-small: 14px;
diff --git a/test/development/client-dev-overlay/app/pages/index.js b/test/development/client-dev-overlay/app/pages/index.js
new file mode 100644
index 0000000000000..95d1ec6405a3c
--- /dev/null
+++ b/test/development/client-dev-overlay/app/pages/index.js
@@ -0,0 +1,12 @@
+import React from 'react'
+
+// Create a runtime error.
+if ('window' in global) {
+  throw Error('example runtime error')
+}
+
+const Page = () => {
+  return <div>client-react-dev-overlay</div>
+}
+
+export default Page
diff --git a/test/development/client-dev-overlay/index.test.ts b/test/development/client-dev-overlay/index.test.ts
new file mode 100644
index 0000000000000..a6763f22cc9be
--- /dev/null
+++ b/test/development/client-dev-overlay/index.test.ts
@@ -0,0 +1,75 @@
+import { createNext, FileRef } from 'e2e-utils'
+import webdriver from 'next-webdriver'
+import { NextInstance } from 'test/lib/next-modes/base'
+import { join } from 'path'
+import { BrowserInterface } from 'test/lib/browsers/base'
+import { check } from 'next-test-utils'
+
+describe('client-dev-overlay', () => {
+  let next: NextInstance
+  let browser: BrowserInterface
+
+  beforeAll(async () => {
+    next = await createNext({
+      files: {
+        pages: new FileRef(join(__dirname, 'app/pages')),
+      },
+    })
+  })
+  beforeEach(async () => {
+    browser = await webdriver(next.url, '')
+  })
+  afterAll(() => next.destroy())
+
+  // The `BrowserInterface.hasElementByCssSelector` cannot be used for elements inside a shadow DOM.
+  function elementExistsInNextJSPortalShadowDOM(selector: string) {
+    return browser.eval(
+      `!!document.querySelector('nextjs-portal').shadowRoot.querySelector('${selector}')`
+    ) as any
+  }
+  const selectors = {
+    fullScreenDialog: '[data-nextjs-dialog]',
+    toast: '[data-nextjs-toast]',
+    minimizeButton: '[data-nextjs-errors-dialog-left-right-close-button]',
+    hideButton: '[data-nextjs-toast-errors-hide-button]',
+  }
+  function getToast() {
+    return browser.elementByCss(selectors.toast)
+  }
+  function getMinimizeButton() {
+    return browser.elementByCss(selectors.minimizeButton)
+  }
+  function getHideButton() {
+    return browser.elementByCss(selectors.hideButton)
+  }
+
+  it('should be able to fullscreen the minimized overlay', async () => {
+    await getMinimizeButton().click()
+    await getToast().click()
+
+    await check(async () => {
+      return (await elementExistsInNextJSPortalShadowDOM(
+        selectors.fullScreenDialog
+      ))
+        ? 'success'
+        : 'missing'
+    }, 'success')
+  })
+
+  it('should be able to minimize the fullscreen overlay', async () => {
+    await getMinimizeButton().click()
+    expect(await elementExistsInNextJSPortalShadowDOM(selectors.toast)).toBe(
+      true
+    )
+  })
+
+  it('should be able to hide the minimized overlay', async () => {
+    await getMinimizeButton().click()
+    await getHideButton().click()
+
+    await check(async () => {
+      const exists = await elementExistsInNextJSPortalShadowDOM('div')
+      return exists ? 'found' : 'success'
+    }, 'success')
+  })
+})