diff --git a/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.spec.ts b/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.spec.ts
index 8a3a7e6fa8d..62f9dbec824 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.spec.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.spec.ts
@@ -29,7 +29,7 @@ describe("AutofillInlineMenuContentService", () => {
     autofillInit = new AutofillInit(
       domQueryService,
       domElementVisibilityService,
-      null,
+      undefined,
       autofillInlineMenuContentService,
     );
     autofillInit.init();
@@ -319,6 +319,8 @@ describe("AutofillInlineMenuContentService", () => {
 
   describe("handleContainerElementMutationObserverUpdate", () => {
     let mockMutationRecord: MockProxy<MutationRecord>;
+    let mockBodyMutationRecord: MockProxy<MutationRecord>;
+    let mockHTMLMutationRecord: MockProxy<MutationRecord>;
     let buttonElement: HTMLElement;
     let listElement: HTMLElement;
     let isInlineMenuListVisibleSpy: jest.SpyInstance;
@@ -329,6 +331,16 @@ describe("AutofillInlineMenuContentService", () => {
       <div class="overlay-list"></div>
       `;
       mockMutationRecord = mock<MutationRecord>({ target: globalThis.document.body } as any);
+      mockHTMLMutationRecord = mock<MutationRecord>({
+        target: globalThis.document.body.parentElement,
+        attributeName: "style",
+        type: "attributes",
+      } as any);
+      mockBodyMutationRecord = mock<MutationRecord>({
+        target: globalThis.document.body,
+        attributeName: "style",
+        type: "attributes",
+      } as any);
       buttonElement = document.querySelector(".overlay-button") as HTMLElement;
       listElement = document.querySelector(".overlay-list") as HTMLElement;
       autofillInlineMenuContentService["buttonElement"] = buttonElement;
@@ -343,6 +355,7 @@ describe("AutofillInlineMenuContentService", () => {
           "isTriggeringExcessiveMutationObserverIterations",
         )
         .mockReturnValue(false);
+      jest.spyOn(autofillInlineMenuContentService as any, "closeInlineMenu");
     });
 
     it("skips handling the mutation if the overlay elements are not present in the DOM", async () => {
@@ -373,6 +386,33 @@ describe("AutofillInlineMenuContentService", () => {
       expect(globalThis.document.body.insertBefore).not.toHaveBeenCalled();
     });
 
+    it("closes the inline menu if the page body is not sufficiently opaque", async () => {
+      document.querySelector("html").style.opacity = "0.9";
+      document.body.style.opacity = "0";
+      autofillInlineMenuContentService["handlePageMutations"]([mockBodyMutationRecord]);
+
+      expect(autofillInlineMenuContentService["pageIsOpaque"]).toBe(false);
+      expect(autofillInlineMenuContentService["closeInlineMenu"]).toHaveBeenCalled();
+    });
+
+    it("closes the inline menu if the page html is not sufficiently opaque", async () => {
+      document.querySelector("html").style.opacity = "0.3";
+      document.body.style.opacity = "0.7";
+      autofillInlineMenuContentService["handlePageMutations"]([mockHTMLMutationRecord]);
+
+      expect(autofillInlineMenuContentService["pageIsOpaque"]).toBe(false);
+      expect(autofillInlineMenuContentService["closeInlineMenu"]).toHaveBeenCalled();
+    });
+
+    it("does not close the inline menu if the page html and body is sufficiently opaque", async () => {
+      document.querySelector("html").style.opacity = "0.9";
+      document.body.style.opacity = "1";
+      autofillInlineMenuContentService["handlePageMutations"]([mockBodyMutationRecord]);
+
+      expect(autofillInlineMenuContentService["pageIsOpaque"]).toBe(true);
+      expect(autofillInlineMenuContentService["closeInlineMenu"]).not.toHaveBeenCalled();
+    });
+
     it("skips re-arranging the DOM elements if the last child of the body is non-existent", async () => {
       document.body.innerHTML = "";
 
diff --git a/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.ts b/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.ts
index 9bdaf0f965b..de401bf7e28 100644
--- a/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.ts
+++ b/apps/browser/src/autofill/overlay/inline-menu/content/autofill-inline-menu-content.service.ts
@@ -29,8 +29,11 @@ export class AutofillInlineMenuContentService implements AutofillInlineMenuConte
   private isFirefoxBrowser =
     globalThis.navigator.userAgent.indexOf(" Firefox/") !== -1 ||
     globalThis.navigator.userAgent.indexOf(" Gecko/") !== -1;
-  private buttonElement: HTMLElement;
-  private listElement: HTMLElement;
+  private buttonElement?: HTMLElement;
+  private listElement?: HTMLElement;
+  private htmlMutationObserver: MutationObserver;
+  private bodyMutationObserver: MutationObserver;
+  private pageIsOpaque = true;
   private inlineMenuElementsMutationObserver: MutationObserver;
   private containerElementMutationObserver: MutationObserver;
   private mutationObserverIterations = 0;
@@ -49,6 +52,7 @@ export class AutofillInlineMenuContentService implements AutofillInlineMenuConte
   };
 
   constructor() {
+    this.checkPageOpacity();
     this.setupMutationObserver();
   }
 
@@ -281,6 +285,9 @@ export class AutofillInlineMenuContentService implements AutofillInlineMenuConte
    * that the inline menu elements are always present at the bottom of the menu container.
    */
   private setupMutationObserver = () => {
+    this.htmlMutationObserver = new MutationObserver(this.handlePageMutations);
+    this.bodyMutationObserver = new MutationObserver(this.handlePageMutations);
+
     this.inlineMenuElementsMutationObserver = new MutationObserver(
       this.handleInlineMenuElementMutationObserverUpdate,
     );
@@ -295,6 +302,9 @@ export class AutofillInlineMenuContentService implements AutofillInlineMenuConte
    * elements are not modified by the website.
    */
   private observeCustomElements() {
+    this.htmlMutationObserver?.observe(document.querySelector("html"), { attributes: true });
+    this.bodyMutationObserver?.observe(document.body, { attributes: true });
+
     if (this.buttonElement) {
       this.inlineMenuElementsMutationObserver?.observe(this.buttonElement, {
         attributes: true,
@@ -395,11 +405,56 @@ export class AutofillInlineMenuContentService implements AutofillInlineMenuConte
     });
   };
 
+  private checkPageOpacity = () => {
+    this.pageIsOpaque = this.getPageIsOpaque();
+
+    if (!this.pageIsOpaque) {
+      this.closeInlineMenu();
+    }
+  };
+
+  private handlePageMutations = (mutations: MutationRecord[]) => {
+    for (const mutation of mutations) {
+      if (mutation.type === "attributes") {
+        this.checkPageOpacity();
+      }
+    }
+  };
+
+  /**
+   * Checks the opacity of the page body and body parent, since the inline menu experience
+   * will inherit the opacity, despite being otherwise encapsulated from styling changes
+   * of parents below the body. Assumes the target element will be a direct child of the page
+   * `body` (enforced elsewhere).
+   */
+  private getPageIsOpaque() {
+    // These are computed style values, so we don't need to worry about non-float values
+    // for `opacity`, here
+    const htmlOpacity = globalThis.window.getComputedStyle(
+      globalThis.document.querySelector("html"),
+    ).opacity;
+    const bodyOpacity = globalThis.window.getComputedStyle(
+      globalThis.document.querySelector("body"),
+    ).opacity;
+
+    // Any value above this is considered "opaque" for our purposes
+    const opacityThreshold = 0.6;
+
+    return parseFloat(htmlOpacity) > opacityThreshold && parseFloat(bodyOpacity) > opacityThreshold;
+  }
+
   /**
    * Processes the mutation of the element that contains the inline menu. Will trigger when an
    * idle moment in the execution of the main thread is detected.
    */
   private processContainerElementMutation = async (containerElement: HTMLElement) => {
+    // If the computed opacity of the body and parent is not sufficiently opaque, tear
+    // down and prevent building the inline menu experience.
+    this.checkPageOpacity();
+    if (!this.pageIsOpaque) {
+      return;
+    }
+
     const lastChild = containerElement.lastElementChild;
     const secondToLastChild = lastChild?.previousElementSibling;
     const lastChildIsInlineMenuList = lastChild === this.listElement;