diff --git a/apps/browser/src/autofill/background/abstractions/overlay.background.ts b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
index 0d3785de321..f5d8257e635 100644
--- a/apps/browser/src/autofill/background/abstractions/overlay.background.ts
+++ b/apps/browser/src/autofill/background/abstractions/overlay.background.ts
@@ -12,9 +12,10 @@ type PageDetailsForTab = Record<
 >;
 
 type SubFrameOffsetData = {
-  url: string;
+  url?: string;
   top: number;
   left: number;
+  frameId?: number;
 } | null;
 
 type SubFrameOffsetsForTab = Record<
@@ -110,6 +111,7 @@ type OverlayBackgroundExtensionMessageHandlers = {
   updateIsFieldCurrentlyFilling: ({ message }: BackgroundMessageParam) => void;
   checkIsInlineMenuButtonVisible: ({ sender }: BackgroundSenderParam) => void;
   checkIsInlineMenuListVisible: ({ sender }: BackgroundSenderParam) => void;
+  updateSubFrameData: ({ message, sender }: BackgroundOnMessageHandlerParams) => void;
 };
 
 type PortMessageParam = {
diff --git a/apps/browser/src/autofill/background/overlay.background.ts b/apps/browser/src/autofill/background/overlay.background.ts
index d4673100e8e..653acd526d8 100644
--- a/apps/browser/src/autofill/background/overlay.background.ts
+++ b/apps/browser/src/autofill/background/overlay.background.ts
@@ -84,6 +84,7 @@ class OverlayBackground implements OverlayBackgroundInterface {
       (this.isCurrentlyFilling = message.isFieldCurrentlyFilling),
     checkIsInlineMenuButtonVisible: ({ sender }) => this.checkIsInlineMenuButtonVisible(sender),
     checkIsInlineMenuListVisible: ({ sender }) => this.checkIsInlineMenuListVisible(sender),
+    updateSubFrameData: ({ message, sender }) => this.updateSubFrameData(message, sender),
   };
   private readonly overlayButtonPortMessageHandlers: OverlayButtonPortMessageHandlers = {
     overlayButtonClicked: ({ port }) => this.handleOverlayButtonClicked(port),
@@ -127,6 +128,13 @@ class OverlayBackground implements OverlayBackgroundInterface {
     return value;
   }
 
+  updateSubFrameData(message: any, sender: chrome.runtime.MessageSender) {
+    const subFrameOffsetsForTab = this.subFrameOffsetsForTab[sender.tab.id];
+    if (subFrameOffsetsForTab) {
+      subFrameOffsetsForTab.set(message.subFrameData.frameId, message.subFrameData);
+    }
+  }
+
   private async checkIsInlineMenuListVisible(sender: chrome.runtime.MessageSender) {
     return await BrowserApi.tabSendMessage(
       sender.tab,
@@ -277,12 +285,26 @@ class OverlayBackground implements OverlayBackgroundInterface {
     while (frameDetails.parentFrameId !== -1) {
       const subFrameOffset: SubFrameOffsetData = await BrowserApi.tabSendMessage(
         tab,
-        { command: "getSubFrameOffsets", subFrameUrl: frameDetails.url },
+        {
+          command: "getSubFrameOffsets",
+          subFrameUrl: frameDetails.url,
+          subFrameId: frameDetails.documentId,
+        },
         { frameId: frameDetails.parentFrameId },
       );
 
       if (!subFrameOffset) {
         subFrameOffsetsForTab.set(frameId, null);
+        void BrowserApi.tabSendMessage(
+          tab,
+          {
+            command: "getSubFrameOffsetsThroughWindowMessaging",
+            subFrameId: frameId,
+          },
+          {
+            frameId: frameId,
+          },
+        );
         return;
       }
 
diff --git a/apps/browser/src/autofill/content/abstractions/autofill-init.ts b/apps/browser/src/autofill/content/abstractions/autofill-init.ts
index da3d58950dd..59e44bfed0c 100644
--- a/apps/browser/src/autofill/content/abstractions/autofill-init.ts
+++ b/apps/browser/src/autofill/content/abstractions/autofill-init.ts
@@ -10,6 +10,7 @@ export type AutofillExtensionMessage = {
   fillScript?: AutofillScript;
   url?: string;
   subFrameUrl?: string;
+  subFrameId?: string;
   pageDetailsUrl?: string;
   ciphers?: any;
   isInlineMenuHidden?: boolean;
@@ -40,6 +41,7 @@ export type AutofillExtensionMessageHandlers = {
   bgVaultItemRepromptPopoutOpened: () => void;
   updateAutofillOverlayVisibility: ({ message }: AutofillExtensionMessageParam) => void;
   getSubFrameOffsets: ({ message }: AutofillExtensionMessageParam) => Promise<SubFrameOffsetData>;
+  getSubFrameOffsetsThroughWindowMessaging: ({ message }: AutofillExtensionMessageParam) => void;
 };
 
 export interface AutofillInit {
diff --git a/apps/browser/src/autofill/content/autofill-init.ts b/apps/browser/src/autofill/content/autofill-init.ts
index c38850938bc..07e7045c0b5 100644
--- a/apps/browser/src/autofill/content/autofill-init.ts
+++ b/apps/browser/src/autofill/content/autofill-init.ts
@@ -33,6 +33,8 @@ class AutofillInit implements AutofillInitInterface {
     bgVaultItemRepromptPopoutOpened: () => this.blurAndRemoveOverlay(),
     updateAutofillOverlayVisibility: ({ message }) => this.updateAutofillOverlayVisibility(message),
     getSubFrameOffsets: ({ message }) => this.getSubFrameOffsets(message),
+    getSubFrameOffsetsThroughWindowMessaging: ({ message }) =>
+      this.getSubFrameOffsetsThroughWindowMessaging(message),
   };
 
   /**
@@ -71,6 +73,45 @@ class AutofillInit implements AutofillInitInterface {
       this.domElementVisibilityService,
       this.collectAutofillContentService,
     );
+
+    window.addEventListener("message", (event) => {
+      // if (event.source !== window) {
+      //   return;
+      // }
+
+      if (event.data.command === "calculateSubFramePositioning") {
+        const subFrameData = event.data.subFrameData;
+        let subFrameOffsets: SubFrameOffsetData;
+        const iframes = document.querySelectorAll("iframe");
+        for (let i = 0; i < iframes.length; i++) {
+          if (iframes[i].contentWindow === event.source) {
+            const iframeElement = iframes[i];
+            subFrameOffsets = this.calculateSubFrameOffsets(
+              iframeElement,
+              subFrameData.url,
+              subFrameData.frameId,
+            );
+
+            subFrameData.top += subFrameOffsets.top;
+            subFrameData.left += subFrameOffsets.left;
+
+            break;
+          }
+        }
+
+        if (globalThis.window.self !== globalThis.window.top) {
+          globalThis.parent.postMessage(
+            { command: "calculateSubFramePositioning", subFrameData },
+            "*",
+          );
+          return;
+        }
+
+        void sendExtensionMessage("updateSubFrameData", {
+          subFrameData,
+        });
+      }
+    });
   }
 
   /**
@@ -245,14 +286,27 @@ class AutofillInit implements AutofillInitInterface {
   ): Promise<SubFrameOffsetData | null> {
     const { subFrameUrl } = message;
     const subFrameUrlWithoutTrailingSlash = subFrameUrl?.replace(/\/$/, "");
-    const iframeElement = document.querySelector(
+
+    let iframeElement: HTMLIFrameElement | null = null;
+    const iframeElements = document.querySelectorAll(
       `iframe[src="${subFrameUrl}"], iframe[src="${subFrameUrlWithoutTrailingSlash}"]`,
-    );
+    ) as NodeListOf<HTMLIFrameElement>;
+    if (iframeElements.length === 1) {
+      iframeElement = iframeElements[0];
+    }
 
     if (!iframeElement) {
       return null;
     }
 
+    return this.calculateSubFrameOffsets(iframeElement, subFrameUrl);
+  }
+
+  private calculateSubFrameOffsets(
+    iframeElement: HTMLIFrameElement,
+    subFrameUrl?: string,
+    frameId?: number,
+  ): SubFrameOffsetData {
     const iframeRect = iframeElement.getBoundingClientRect();
     const iframeStyles = globalThis.getComputedStyle(iframeElement);
     const paddingLeft = parseInt(iframeStyles.getPropertyValue("padding-left"));
@@ -262,11 +316,27 @@ class AutofillInit implements AutofillInitInterface {
 
     return {
       url: subFrameUrl,
+      frameId,
       top: iframeRect.top + paddingTop + borderWidthTop,
       left: iframeRect.left + paddingLeft + borderWidthLeft,
     };
   }
 
+  private getSubFrameOffsetsThroughWindowMessaging(message: any) {
+    globalThis.parent.postMessage(
+      {
+        command: "calculateSubFramePositioning",
+        subFrameData: {
+          url: window.location.href,
+          frameId: message.subFrameId,
+          left: 0,
+          top: 0,
+        },
+      },
+      "*",
+    );
+  }
+
   /**
    * Sets up the extension message listeners for the content script.
    */