diff --git a/apps/browser/src/platform/popup/layout/popup-header.component.html b/apps/browser/src/platform/popup/layout/popup-header.component.html
index e866ba4e81..31cd126532 100644
--- a/apps/browser/src/platform/popup/layout/popup-header.component.html
+++ b/apps/browser/src/platform/popup/layout/popup-header.component.html
@@ -1,5 +1,11 @@
 <header
-  class="tw-p-4 tw-border-0 tw-border-solid tw-border-b tw-border-secondary-300 tw-bg-background"
+  class="tw-p-4 tw-transition-colors tw-duration-200 tw-border-0 tw-border-b tw-border-solid"
+  [ngClass]="{
+    'tw-bg-background-alt tw-border-transparent':
+      this.background === 'alt' && !pageContentScrolled(),
+    'tw-bg-background tw-border-secondary-300':
+      (this.background === 'alt' && pageContentScrolled()) || this.background === 'default'
+  }"
 >
   <div class="tw-max-w-screen-sm tw-mx-auto tw-flex tw-justify-between tw-w-full">
     <div class="tw-inline-flex tw-items-center tw-gap-2 tw-h-9">
@@ -11,7 +17,10 @@
         [ariaLabel]="'back' | i18n"
         [bitAction]="backAction"
       ></button>
-      <h1 bitTypography="h3" class="!tw-mb-0.5 tw-text-headers">{{ pageTitle }}</h1>
+      <h1 *ngIf="pageTitle" bitTypography="h3" class="!tw-mb-0.5 tw-text-headers">
+        {{ pageTitle }}
+      </h1>
+      <ng-content></ng-content>
     </div>
     <div class="tw-inline-flex tw-items-center tw-gap-2 tw-h-9">
       <ng-content select="[slot=end]"></ng-content>
diff --git a/apps/browser/src/platform/popup/layout/popup-header.component.ts b/apps/browser/src/platform/popup/layout/popup-header.component.ts
index 1b491ea881..1e41f7ccbe 100644
--- a/apps/browser/src/platform/popup/layout/popup-header.component.ts
+++ b/apps/browser/src/platform/popup/layout/popup-header.component.ts
@@ -1,6 +1,6 @@
 import { BooleanInput, coerceBooleanProperty } from "@angular/cdk/coercion";
 import { CommonModule, Location } from "@angular/common";
-import { Component, Input } from "@angular/core";
+import { Component, Input, Signal, inject } from "@angular/core";
 
 import { JslibModule } from "@bitwarden/angular/jslib.module";
 import {
@@ -10,6 +10,8 @@ import {
   TypographyModule,
 } from "@bitwarden/components";
 
+import { PopupPageComponent } from "./popup-page.component";
+
 @Component({
   selector: "popup-header",
   templateUrl: "popup-header.component.html",
@@ -17,6 +19,12 @@ import {
   imports: [TypographyModule, CommonModule, IconButtonModule, JslibModule, AsyncActionsModule],
 })
 export class PopupHeaderComponent {
+  protected pageContentScrolled: Signal<boolean> = inject(PopupPageComponent).isScrolled;
+
+  /** Background color */
+  @Input()
+  background: "default" | "alt" = "default";
+
   /** Display the back button, which uses Location.back() to go back one page in history */
   @Input()
   get showBackButton() {
diff --git a/apps/browser/src/platform/popup/layout/popup-layout.mdx b/apps/browser/src/platform/popup/layout/popup-layout.mdx
index 49f76501ae..aa11b4099a 100644
--- a/apps/browser/src/platform/popup/layout/popup-layout.mdx
+++ b/apps/browser/src/platform/popup/layout/popup-layout.mdx
@@ -74,6 +74,9 @@ Basic usage example:
 - `showBackButton`: optional, defaults to `false`
   - Toggles the back button to appear. The back button uses `Location.back()` to navigate back one
     page in history.
+- `background`: optional
+  - `"default"` uses a white background
+  - `"alt"` uses a transparent background
 
 **Slots**
 
@@ -92,6 +95,12 @@ Usage example:
 </popup-header>
 ```
 
+### Transparent header
+
+<Canvas>
+  <Story of={stories.TransparentHeader} />
+</Canvas>
+
 Common interactive elements to insert into the `end` slot are:
 
 - `app-current-account`: shows current account and switcher
diff --git a/apps/browser/src/platform/popup/layout/popup-layout.stories.ts b/apps/browser/src/platform/popup/layout/popup-layout.stories.ts
index 408988dca3..3d067b5305 100644
--- a/apps/browser/src/platform/popup/layout/popup-layout.stories.ts
+++ b/apps/browser/src/platform/popup/layout/popup-layout.stories.ts
@@ -303,6 +303,7 @@ export default {
         MockSettingsPageComponent,
         MockVaultPagePoppedComponent,
         NoItemsModule,
+        VaultComponent,
       ],
       providers: [
         {
@@ -311,6 +312,7 @@ export default {
             return new I18nMockService({
               back: "Back",
               loading: "Loading",
+              search: "Search",
             });
           },
         },
@@ -421,3 +423,20 @@ export const Loading: Story = {
     `,
   }),
 };
+
+export const TransparentHeader: Story = {
+  render: (args) => ({
+    props: args,
+    template: /* HTML */ `
+      <extension-container>
+        <popup-page>
+          <popup-header slot="header" background="alt"
+            ><span class="tw-italic tw-text-main">🤠 Custom Content</span></popup-header
+          >
+
+          <vault-placeholder></vault-placeholder>
+        </popup-page>
+      </extension-container>
+    `,
+  }),
+};
diff --git a/apps/browser/src/platform/popup/layout/popup-page.component.html b/apps/browser/src/platform/popup/layout/popup-page.component.html
index d53ef24803..e62f9e70f9 100644
--- a/apps/browser/src/platform/popup/layout/popup-page.component.html
+++ b/apps/browser/src/platform/popup/layout/popup-page.component.html
@@ -1,20 +1,21 @@
 <ng-content select="[slot=header]"></ng-content>
 <main class="tw-flex-1 tw-overflow-hidden tw-flex tw-flex-col tw-relative tw-bg-background-alt">
-  <div #nonScrollable [ngClass]="{ 'tw-invisible': loading }">
+  <div
+    #nonScrollable
+    class="tw-transition-colors tw-duration-200 tw-border-0 tw-border-b tw-border-solid"
+    [ngClass]="{
+      'tw-invisible': loading || nonScrollable.childElementCount === 0,
+      'tw-border-secondary-300': scrolled(),
+      'tw-border-transparent': !scrolled()
+    }"
+  >
     <ng-content select="[slot=above-scroll-area]"></ng-content>
   </div>
   <div
     class="tw-max-w-screen-sm tw-mx-auto tw-overflow-y-auto tw-flex tw-flex-col tw-w-full tw-h-full"
+    (scroll)="handleScroll($event)"
     [ngClass]="{ 'tw-invisible': loading }"
   >
-    <!-- Only shown when the `slot=above-scroll-area` is populated -->
-    <!-- The first div will "stick" and show a bottom border when content is scrolled -->
-    <!-- The second div is displayed on top of the first to hide it until the content is scrolled -->
-    <ng-container *ngIf="nonScrollable.children.length">
-      <div class="tw-sticky tw-min-h-[1px] tw-bg-secondary-300 tw-top-0"></div>
-      <div class="tw-relative tw-z-10 tw-min-h-[2px] tw-bg-background-alt -tw-mt-[2px]"></div>
-    </ng-container>
-
     <div
       class="tw-max-w-screen-sm tw-mx-auto tw-p-3 tw-flex-1 tw-flex tw-flex-col tw-h-full tw-w-full"
     >
diff --git a/apps/browser/src/platform/popup/layout/popup-page.component.ts b/apps/browser/src/platform/popup/layout/popup-page.component.ts
index 0ce13ac4a4..50db3e370f 100644
--- a/apps/browser/src/platform/popup/layout/popup-page.component.ts
+++ b/apps/browser/src/platform/popup/layout/popup-page.component.ts
@@ -1,5 +1,5 @@
 import { CommonModule } from "@angular/common";
-import { Component, Input, inject } from "@angular/core";
+import { Component, Input, inject, signal } from "@angular/core";
 
 import { I18nService } from "@bitwarden/common/platform/abstractions/i18n.service";
 
@@ -17,6 +17,13 @@ export class PopupPageComponent {
 
   @Input() loading = false;
 
+  protected scrolled = signal(false);
+  isScrolled = this.scrolled.asReadonly();
+
   /** Accessible loading label for the spinner. Defaults to "loading" */
   @Input() loadingText?: string = this.i18nService.t("loading");
+
+  handleScroll(event: Event) {
+    this.scrolled.set((event.currentTarget as HTMLElement).scrollTop !== 0);
+  }
 }