diff --git a/apps/browser/src/platform/popup/layout/popup-layout.mdx b/apps/browser/src/platform/popup/layout/popup-layout.mdx
index b805805ad18..49f76501aea 100644
--- a/apps/browser/src/platform/popup/layout/popup-layout.mdx
+++ b/apps/browser/src/platform/popup/layout/popup-layout.mdx
@@ -41,6 +41,9 @@ page looks nice when the extension is popped out.
 - `footer`
   - Use the `popup-footer` component.
   - Not every page will have a footer.
+- `above-scroll-area`
+  - When the page content overflows, this content will be "stuck" to the top of the page upon
+    scrolling.
 - default
   - Whatever content you want in `main`.
 
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 f2208a8b8f5..9857eeccc31 100644
--- a/apps/browser/src/platform/popup/layout/popup-layout.stories.ts
+++ b/apps/browser/src/platform/popup/layout/popup-layout.stories.ts
@@ -12,6 +12,7 @@ import {
   IconButtonModule,
   ItemModule,
   NoItemsModule,
+  SearchModule,
 } from "@bitwarden/components";
 
 import { PopupFooterComponent } from "./popup-footer.component";
@@ -103,6 +104,18 @@ class MockPopoutButtonComponent {}
 })
 class MockCurrentAccountComponent {}
 
+@Component({
+  selector: "mock-search",
+  template: `
+    <div class="tw-p-4">
+      <bit-search placeholder="Search"> </bit-search>
+    </div>
+  `,
+  standalone: true,
+  imports: [SearchModule],
+})
+class MockSearchComponent {}
+
 @Component({
   selector: "mock-vault-page",
   template: `
@@ -114,6 +127,7 @@ class MockCurrentAccountComponent {}
           <mock-current-account></mock-current-account>
         </ng-container>
       </popup-header>
+      <mock-search slot="above-scroll-area"></mock-search>
       <vault-placeholder></vault-placeholder>
     </popup-page>
   `,
@@ -124,6 +138,7 @@ class MockCurrentAccountComponent {}
     MockAddButtonComponent,
     MockPopoutButtonComponent,
     MockCurrentAccountComponent,
+    MockSearchComponent,
     VaultComponent,
   ],
 })
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 87f91e781a7..d53ef24803d 100644
--- a/apps/browser/src/platform/popup/layout/popup-page.component.html
+++ b/apps/browser/src/platform/popup/layout/popup-page.component.html
@@ -1,10 +1,25 @@
 <ng-content select="[slot=header]"></ng-content>
-<main class="tw-flex-1 tw-overflow-y-auto tw-h-full tw-relative tw-bg-background-alt">
+<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 }">
+    <ng-content select="[slot=above-scroll-area]"></ng-content>
+  </div>
   <div
-    class="tw-max-w-screen-sm tw-mx-auto tw-p-3 tw-overflow-y-auto tw-h-full"
+    class="tw-max-w-screen-sm tw-mx-auto tw-overflow-y-auto tw-flex tw-flex-col tw-w-full tw-h-full"
     [ngClass]="{ 'tw-invisible': loading }"
   >
-    <ng-content></ng-content>
+    <!-- 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"
+    >
+      <ng-content></ng-content>
+    </div>
   </div>
   <span
     class="tw-absolute tw-inset-0 tw-flex tw-items-center tw-justify-center tw-text-main"
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 97a67fc852c..0ce13ac4a49 100644
--- a/apps/browser/src/platform/popup/layout/popup-page.component.ts
+++ b/apps/browser/src/platform/popup/layout/popup-page.component.ts
@@ -8,7 +8,7 @@ import { I18nService } from "@bitwarden/common/platform/abstractions/i18n.servic
   templateUrl: "popup-page.component.html",
   standalone: true,
   host: {
-    class: "tw-h-full tw-flex tw-flex-col tw-flex-1 tw-overflow-y-auto",
+    class: "tw-h-full tw-flex tw-flex-col tw-flex-1 tw-overflow-y-hidden",
   },
   imports: [CommonModule],
 })
diff --git a/apps/browser/src/vault/popup/components/vault-v2/vault-list-filters/vault-list-filters.component.html b/apps/browser/src/vault/popup/components/vault-v2/vault-list-filters/vault-list-filters.component.html
index 32427ac2da6..0e241a81dcb 100644
--- a/apps/browser/src/vault/popup/components/vault-v2/vault-list-filters/vault-list-filters.component.html
+++ b/apps/browser/src/vault/popup/components/vault-v2/vault-list-filters/vault-list-filters.component.html
@@ -1,5 +1,5 @@
 <div role="toolbar" [ariaLabel]="'filters' | i18n">
-  <form [formGroup]="filterForm" class="tw-flex tw-flex-wrap tw-gap-2 tw-mb-6 tw-mt-2">
+  <form [formGroup]="filterForm" class="tw-flex tw-flex-wrap tw-gap-2 tw-mt-2">
     <ng-container *ngIf="organizations$ | async as organizations">
       <bit-chip-select
         *ngIf="organizations.length"
diff --git a/apps/browser/src/vault/popup/components/vault/vault-v2.component.html b/apps/browser/src/vault/popup/components/vault/vault-v2.component.html
index f666bc09a89..6422bc3c84b 100644
--- a/apps/browser/src/vault/popup/components/vault/vault-v2.component.html
+++ b/apps/browser/src/vault/popup/components/vault/vault-v2.component.html
@@ -22,10 +22,13 @@
     </bit-no-items>
   </div>
 
-  <ng-container *ngIf="vaultState !== VaultStateEnum.Empty">
+  <!-- Show search & filters outside of the scroll area of the page -->
+  <div slot="above-scroll-area" class="tw-p-4" *ngIf="vaultState !== VaultStateEnum.Empty">
     <app-vault-v2-search> </app-vault-v2-search>
-
     <app-vault-list-filters></app-vault-list-filters>
+  </div>
+
+  <ng-container *ngIf="vaultState !== VaultStateEnum.Empty">
     <div
       *ngIf="vaultState === VaultStateEnum.NoResults"
       class="tw-flex tw-flex-col tw-justify-center tw-h-auto tw-pt-12"