diff --git a/apps/browser/src/autofill/fido2/background/fido2.background.spec.ts b/apps/browser/src/autofill/fido2/background/fido2.background.spec.ts
index f0c5fc5695..43d07bdea1 100644
--- a/apps/browser/src/autofill/fido2/background/fido2.background.spec.ts
+++ b/apps/browser/src/autofill/fido2/background/fido2.background.spec.ts
@@ -32,7 +32,7 @@ const contentScriptDetails = {
   ...sharedScriptInjectionDetails,
 };
 const sharedRegistrationOptions = {
-  matches: ["https://*/*"],
+  matches: ["https://*/*", "http://localhost/*"],
   excludeMatches: ["https://*/*.xml*"],
   allFrames: true,
   ...sharedExecuteScriptOptions,
diff --git a/apps/browser/src/autofill/fido2/background/fido2.background.ts b/apps/browser/src/autofill/fido2/background/fido2.background.ts
index a58d32da16..0524a2529f 100644
--- a/apps/browser/src/autofill/fido2/background/fido2.background.ts
+++ b/apps/browser/src/autofill/fido2/background/fido2.background.ts
@@ -33,7 +33,7 @@ export class Fido2Background implements Fido2BackgroundInterface {
     runAt: "document_start",
   };
   private readonly sharedRegistrationOptions: SharedFido2ScriptRegistrationOptions = {
-    matches: ["https://*/*"],
+    matches: ["https://*/*", "http://localhost/*"],
     excludeMatches: ["https://*/*.xml*"],
     allFrames: true,
     ...this.sharedInjectionDetails,
diff --git a/apps/browser/src/autofill/fido2/content/fido2-content-script.ts b/apps/browser/src/autofill/fido2/content/fido2-content-script.ts
index ad9f526f6c..171aa7cd83 100644
--- a/apps/browser/src/autofill/fido2/content/fido2-content-script.ts
+++ b/apps/browser/src/autofill/fido2/content/fido2-content-script.ts
@@ -17,7 +17,9 @@ import { MessageWithMetadata, Messenger } from "./messaging/messenger";
 (function (globalContext) {
   const shouldExecuteContentScript =
     globalContext.document.contentType === "text/html" &&
-    globalContext.document.location.protocol === "https:";
+    (globalContext.document.location.protocol === "https:" ||
+      (globalContext.document.location.protocol === "http:" &&
+        globalContext.document.location.hostname === "localhost"));
 
   if (!shouldExecuteContentScript) {
     return;
diff --git a/apps/browser/src/autofill/fido2/content/fido2-page-script.ts b/apps/browser/src/autofill/fido2/content/fido2-page-script.ts
index cf14471359..5f91e6c081 100644
--- a/apps/browser/src/autofill/fido2/content/fido2-page-script.ts
+++ b/apps/browser/src/autofill/fido2/content/fido2-page-script.ts
@@ -8,7 +8,9 @@ import { Messenger } from "./messaging/messenger";
 (function (globalContext) {
   const shouldExecuteContentScript =
     globalContext.document.contentType === "text/html" &&
-    globalContext.document.location.protocol === "https:";
+    (globalContext.document.location.protocol === "https:" ||
+      (globalContext.document.location.protocol === "http:" &&
+        globalContext.document.location.hostname === "localhost"));
 
   if (!shouldExecuteContentScript) {
     return;
diff --git a/apps/browser/src/autofill/fido2/content/fido2-page-script.webauthn-supported.spec.ts b/apps/browser/src/autofill/fido2/content/fido2-page-script.webauthn-supported.spec.ts
index 46ef4d60d6..292d0e0118 100644
--- a/apps/browser/src/autofill/fido2/content/fido2-page-script.webauthn-supported.spec.ts
+++ b/apps/browser/src/autofill/fido2/content/fido2-page-script.webauthn-supported.spec.ts
@@ -16,8 +16,9 @@ const mockGlobalThisDocument = {
   contentType: "text/html",
   location: {
     ...originalGlobalThis.document.location,
-    href: "https://localhost",
-    origin: "https://localhost",
+    href: "https://bitwarden.com",
+    origin: "https://bitwarden.com",
+    hostname: "bitwarden.com",
     protocol: "https:",
   },
 };
@@ -166,8 +167,8 @@ describe("Fido2 page script with native WebAuthn support", () => {
         ...mockGlobalThisDocument,
         location: {
           ...mockGlobalThisDocument.location,
-          href: "http://localhost",
-          origin: "http://localhost",
+          href: "http://bitwarden.com",
+          origin: "http://bitwarden.com",
           protocol: "http:",
         },
       }));
diff --git a/libs/common/src/platform/services/fido2/fido2-client.service.spec.ts b/libs/common/src/platform/services/fido2/fido2-client.service.spec.ts
index 13e1d8f282..597f2d8f32 100644
--- a/libs/common/src/platform/services/fido2/fido2-client.service.spec.ts
+++ b/libs/common/src/platform/services/fido2/fido2-client.service.spec.ts
@@ -19,6 +19,7 @@ import {
 } from "../../abstractions/fido2/fido2-client.service.abstraction";
 import { Utils } from "../../misc/utils";
 
+import * as DomainUtils from "./domain-utils";
 import { Fido2AuthenticatorService } from "./fido2-authenticator.service";
 import { Fido2ClientService } from "./fido2-client.service";
 import { Fido2Utils } from "./fido2-utils";
@@ -36,6 +37,7 @@ describe("FidoAuthenticatorService", () => {
   let domainSettingsService: MockProxy<DomainSettingsService>;
   let client!: Fido2ClientService;
   let tab!: chrome.tabs.Tab;
+  let isValidRpId!: jest.SpyInstance;
 
   beforeEach(async () => {
     authenticator = mock<Fido2AuthenticatorService>();
@@ -44,6 +46,8 @@ describe("FidoAuthenticatorService", () => {
     vaultSettingsService = mock<VaultSettingsService>();
     domainSettingsService = mock<DomainSettingsService>();
 
+    isValidRpId = jest.spyOn(DomainUtils, "isValidRpId");
+
     client = new Fido2ClientService(
       authenticator,
       configService,
@@ -58,6 +62,10 @@ describe("FidoAuthenticatorService", () => {
     tab = { id: 123, windowId: 456 } as chrome.tabs.Tab;
   });
 
+  afterEach(() => {
+    isValidRpId.mockRestore();
+  });
+
   describe("createCredential", () => {
     describe("input parameters validation", () => {
       // Spec: If sameOriginWithAncestors is false, return a "NotAllowedError" DOMException.
@@ -113,6 +121,7 @@ describe("FidoAuthenticatorService", () => {
       });
 
       // Spec: If options.rp.id is not a registrable domain suffix of and is not equal to effectiveDomain, return a DOMException whose name is "SecurityError", and terminate this algorithm.
+      // This is actually checked by `isValidRpId` function, but we'll test it here as well
       it("should throw error if rp.id is not valid for this origin", async () => {
         const params = createParams({
           origin: "https://passwordless.dev",
@@ -126,6 +135,20 @@ describe("FidoAuthenticatorService", () => {
         await rejects.toBeInstanceOf(DOMException);
       });
 
+      // Sanity check to make sure that we use `isValidRpId` to validate the rp.id
+      it("should throw if isValidRpId returns false", async () => {
+        const params = createParams();
+        authenticator.makeCredential.mockResolvedValue(createAuthenticatorMakeResult());
+        // `params` actually has a valid rp.id, but we're mocking the function to return false
+        isValidRpId.mockReturnValue(false);
+
+        const result = async () => await client.createCredential(params, tab);
+
+        const rejects = expect(result).rejects;
+        await rejects.toMatchObject({ name: "SecurityError" });
+        await rejects.toBeInstanceOf(DOMException);
+      });
+
       it("should fallback if origin hostname is found in neverDomains", async () => {
         const params = createParams({
           origin: "https://bitwarden.com",
@@ -151,6 +174,16 @@ describe("FidoAuthenticatorService", () => {
         await rejects.toBeInstanceOf(DOMException);
       });
 
+      it("should not throw error if localhost is http", async () => {
+        const params = createParams({
+          origin: "http://localhost",
+          rp: { id: undefined, name: "localhost" },
+        });
+        authenticator.makeCredential.mockResolvedValue(createAuthenticatorMakeResult());
+
+        await client.createCredential(params, tab);
+      });
+
       // Spec: If credTypesAndPubKeyAlgs is empty, return a DOMException whose name is "NotSupportedError", and terminate this algorithm.
       it("should throw error if no support key algorithms were found", async () => {
         const params = createParams({
@@ -360,6 +393,7 @@ describe("FidoAuthenticatorService", () => {
       });
 
       // Spec: If options.rp.id is not a registrable domain suffix of and is not equal to effectiveDomain, return a DOMException whose name is "SecurityError", and terminate this algorithm.
+      // This is actually checked by `isValidRpId` function, but we'll test it here as well
       it("should throw error if rp.id is not valid for this origin", async () => {
         const params = createParams({
           origin: "https://passwordless.dev",
@@ -373,6 +407,20 @@ describe("FidoAuthenticatorService", () => {
         await rejects.toBeInstanceOf(DOMException);
       });
 
+      // Sanity check to make sure that we use `isValidRpId` to validate the rp.id
+      it("should throw if isValidRpId returns false", async () => {
+        const params = createParams();
+        authenticator.getAssertion.mockResolvedValue(createAuthenticatorAssertResult());
+        // `params` actually has a valid rp.id, but we're mocking the function to return false
+        isValidRpId.mockReturnValue(false);
+
+        const result = async () => await client.assertCredential(params, tab);
+
+        const rejects = expect(result).rejects;
+        await rejects.toMatchObject({ name: "SecurityError" });
+        await rejects.toBeInstanceOf(DOMException);
+      });
+
       it("should fallback if origin hostname is found in neverDomains", async () => {
         const params = createParams({
           origin: "https://bitwarden.com",
@@ -506,6 +554,16 @@ describe("FidoAuthenticatorService", () => {
           expect.anything(),
         );
       });
+
+      it("should not throw error if localhost is http", async () => {
+        const params = createParams({
+          origin: "http://localhost",
+        });
+        params.rpId = undefined;
+        authenticator.getAssertion.mockResolvedValue(createAuthenticatorAssertResult());
+
+        await client.assertCredential(params, tab);
+      });
     });
 
     describe("assert discoverable credential", () => {
diff --git a/libs/common/src/platform/services/fido2/fido2-client.service.ts b/libs/common/src/platform/services/fido2/fido2-client.service.ts
index 5b6a13bc3f..d22b91fda0 100644
--- a/libs/common/src/platform/services/fido2/fido2-client.service.ts
+++ b/libs/common/src/platform/services/fido2/fido2-client.service.ts
@@ -103,7 +103,10 @@ export class Fido2ClientService implements Fido2ClientServiceAbstraction {
     }
 
     params.rp.id = params.rp.id ?? parsedOrigin.hostname;
-    if (parsedOrigin.hostname == undefined || !params.origin.startsWith("https://")) {
+    if (
+      parsedOrigin.hostname == undefined ||
+      (!params.origin.startsWith("https://") && parsedOrigin.hostname !== "localhost")
+    ) {
       this.logService?.warning(`[Fido2Client] Invalid https origin: ${params.origin}`);
       throw new DOMException("'origin' is not a valid https origin", "SecurityError");
     }
@@ -238,7 +241,10 @@ export class Fido2ClientService implements Fido2ClientServiceAbstraction {
 
     params.rpId = params.rpId ?? parsedOrigin.hostname;
 
-    if (parsedOrigin.hostname == undefined || !params.origin.startsWith("https://")) {
+    if (
+      parsedOrigin.hostname == undefined ||
+      (!params.origin.startsWith("https://") && parsedOrigin.hostname !== "localhost")
+    ) {
       this.logService?.warning(`[Fido2Client] Invalid https origin: ${params.origin}`);
       throw new DOMException("'origin' is not a valid https origin", "SecurityError");
     }