diff --git a/server/src/__tests__/better-auth.test.ts b/server/src/__tests__/better-auth.test.ts
index 50aebc6dfad..31798ea7e2b 100644
--- a/server/src/__tests__/better-auth.test.ts
+++ b/server/src/__tests__/better-auth.test.ts
@@ -179,6 +179,35 @@ describe("Better Auth cookie scoping", () => {
     })).toBe(false);
   });
 
+  it("disables secure cookies only for HTTP loopback requests in a managed HTTPS runtime", () => {
+    const managedRuntimeInput = {
+      deploymentMode: "authenticated",
+      deploymentExposure: "private",
+      authBaseUrlMode: "explicit",
+      authPublicBaseUrl: "https://worktree.example.test",
+      publicUrl: "https://worktree.example.test",
+      managedRuntimePublicUrl: "https://worktree.example.test",
+    } as const;
+
+    expect(shouldDisableSecureAuthCookies({
+      ...managedRuntimeInput,
+      requestUrl: "http://127.0.0.1:42013/api/auth/sign-in/email",
+    } as Parameters<typeof shouldDisableSecureAuthCookies>[0])).toBe(true);
+    expect(shouldDisableSecureAuthCookies({
+      ...managedRuntimeInput,
+      requestUrl: "https://worktree.example.test/api/auth/sign-in/email",
+    } as Parameters<typeof shouldDisableSecureAuthCookies>[0])).toBe(false);
+    expect(shouldDisableSecureAuthCookies({
+      ...managedRuntimeInput,
+      managedRuntimePublicUrl: undefined,
+      requestUrl: "http://127.0.0.1:42013/api/auth/sign-in/email",
+    } as Parameters<typeof shouldDisableSecureAuthCookies>[0])).toBe(false);
+    expect(shouldDisableSecureAuthCookies({
+      ...managedRuntimeInput,
+      requestUrl: "http://board.example.test:42013/api/auth/sign-in/email",
+    } as Parameters<typeof shouldDisableSecureAuthCookies>[0])).toBe(false);
+  });
+
   it("adds hostname port variants for authenticated mode on non-default ports", () => {
     const trustedOrigins = deriveAuthTrustedOrigins({
       deploymentMode: "authenticated",
diff --git a/server/src/__tests__/managed-loopback-auth.test.ts b/server/src/__tests__/managed-loopback-auth.test.ts
new file mode 100644
index 00000000000..9b3ee704606
--- /dev/null
+++ b/server/src/__tests__/managed-loopback-auth.test.ts
@@ -0,0 +1,101 @@
+import { createDb } from "@paperclipai/db";
+import { afterAll, beforeAll, describe, expect, it, vi } from "vitest";
+import type { Config } from "../config.js";
+import { createBetterAuthInstance } from "../auth/better-auth.js";
+import {
+  getEmbeddedPostgresTestSupport,
+  startEmbeddedPostgresTestDatabase,
+} from "./helpers/embedded-postgres.js";
+
+const embeddedPostgresSupport = await getEmbeddedPostgresTestSupport();
+const describeEmbeddedPostgres = embeddedPostgresSupport.supported ? describe : describe.skip;
+
+if (!embeddedPostgresSupport.supported) {
+  console.warn(
+    `Skipping managed loopback auth tests on this host: ${embeddedPostgresSupport.reason ?? "unsupported environment"}`,
+  );
+}
+
+function authRequest(origin: string, path: string, init?: RequestInit): Request {
+  return new Request(`${origin}/api/auth${path}`, {
+    ...init,
+    headers: {
+      origin,
+      "content-type": "application/json",
+      ...init?.headers,
+    },
+  });
+}
+
+function sessionCookie(response: Response): string {
+  const cookie = response.headers
+    .getSetCookie()
+    .find((value) => value.includes(".session_token="));
+  expect(cookie).toBeDefined();
+  return cookie!;
+}
+
+describeEmbeddedPostgres("managed runtime loopback auth cookies", () => {
+  const publicOrigin = "https://worktree.example.test";
+  const loopbackOrigin = "http://127.0.0.1:42013";
+  let tempDb: Awaited<ReturnType<typeof startEmbeddedPostgresTestDatabase>> | null = null;
+
+  beforeAll(async () => {
+    tempDb = await startEmbeddedPostgresTestDatabase("paperclip-managed-loopback-auth-");
+  }, 20_000);
+
+  afterAll(async () => {
+    vi.unstubAllEnvs();
+    await tempDb?.cleanup();
+  });
+
+  it("uses a loopback sign-in cookie on the next request while keeping the public cookie secure", async () => {
+    vi.stubEnv("BETTER_AUTH_SECRET", "managed-loopback-auth-test-secret");
+    vi.stubEnv("PAPERCLIP_MANAGED_RUNTIME_PUBLIC_URL", publicOrigin);
+    vi.stubEnv("PAPERCLIP_PUBLIC_URL", "");
+
+    const db = createDb(tempDb!.connectionString);
+    const config = {
+      deploymentMode: "authenticated",
+      deploymentExposure: "private",
+      authBaseUrlMode: "explicit",
+      authPublicBaseUrl: publicOrigin,
+      authDisableSignUp: false,
+    } as Config;
+    const auth = createBetterAuthInstance(db, config, [publicOrigin, loopbackOrigin]);
+    const credentials = {
+      name: "Loopback Operator",
+      email: "loopback-operator@example.test",
+      password: "correct-horse-battery-staple",
+    };
+
+    const signUpResponse = await auth.handler(authRequest(publicOrigin, "/sign-up/email", {
+      method: "POST",
+      body: JSON.stringify(credentials),
+    }));
+    expect(signUpResponse.status).toBe(200);
+    expect(sessionCookie(signUpResponse)).toMatch(/;\s*Secure(?:;|$)/i);
+
+    const signInResponse = await auth.handler(authRequest(loopbackOrigin, "/sign-in/email", {
+      method: "POST",
+      body: JSON.stringify({
+        email: credentials.email,
+        password: credentials.password,
+      }),
+    }));
+    expect(signInResponse.status).toBe(200);
+    const loopbackCookie = sessionCookie(signInResponse);
+    expect(loopbackCookie).not.toMatch(/;\s*Secure(?:;|$)/i);
+
+    const getSessionResponse = await auth.handler(authRequest(loopbackOrigin, "/get-session", {
+      method: "GET",
+      headers: {
+        cookie: loopbackCookie.split(";", 1)[0],
+      },
+    }));
+    expect(getSessionResponse.status).toBe(200);
+    await expect(getSessionResponse.json()).resolves.toMatchObject({
+      user: { email: credentials.email },
+    });
+  });
+});
diff --git a/server/src/auth/better-auth.ts b/server/src/auth/better-auth.ts
index c367ffd3ac7..6fd400a6ec3 100644
--- a/server/src/auth/better-auth.ts
+++ b/server/src/auth/better-auth.ts
@@ -92,11 +92,21 @@ export function shouldDisableSecureAuthCookies(input: {
   authBaseUrlMode: Config["authBaseUrlMode"];
   authPublicBaseUrl: string | undefined;
   publicUrl?: string | undefined;
+  managedRuntimePublicUrl?: string | undefined;
+  requestUrl?: string | undefined;
 }): boolean {
   const publicUrl = (
     input.publicUrl?.trim() ||
     (input.authBaseUrlMode === "explicit" ? input.authPublicBaseUrl?.trim() : "")
   );
+  if (
+    input.deploymentMode === "authenticated" &&
+    isHttpsUrl(publicUrl) &&
+    isHttpsUrl(input.managedRuntimePublicUrl) &&
+    isHttpLoopbackUrl(input.requestUrl)
+  ) {
+    return true;
+  }
   if (publicUrl) return publicUrl.startsWith("http://");
 
   return (
@@ -108,6 +118,52 @@ export function shouldDisableSecureAuthCookies(input: {
   );
 }
 
+function isHttpsUrl(value: string | undefined): boolean {
+  if (!value) return false;
+  try {
+    return new URL(value).protocol === "https:";
+  } catch {
+    return false;
+  }
+}
+
+function isLoopbackHostname(hostname: string): boolean {
+  const normalized = hostname.trim().toLowerCase();
+  return (
+    normalized === "localhost" ||
+    normalized === "127.0.0.1" ||
+    normalized === "[::1]" ||
+    normalized === "::1"
+  );
+}
+
+function isHttpLoopbackUrl(value: string | undefined): boolean {
+  if (!value) return false;
+  try {
+    const url = new URL(value);
+    return url.protocol === "http:" && isLoopbackHostname(url.hostname);
+  } catch {
+    return false;
+  }
+}
+
+function requestUrlFromHeaders(headers: Headers): string | undefined {
+  const host = headers.get("host")?.trim();
+  if (!host) return undefined;
+
+  const forwardedProtocol = headers.get("x-forwarded-proto")?.split(",", 1)[0]?.trim().toLowerCase();
+  const protocol = forwardedProtocol === "http" || forwardedProtocol === "https"
+    ? forwardedProtocol
+    : (() => {
+      try {
+        return isLoopbackHostname(new URL(`http://${host}`).hostname) ? "http" : "https";
+      } catch {
+        return "https";
+      }
+    })();
+  return `${protocol}://${host}`;
+}
+
 function headersFromNodeHeaders(rawHeaders: IncomingHttpHeaders): Headers {
   const headers = new Headers();
   for (const [key, raw] of Object.entries(rawHeaders)) {
@@ -185,6 +241,7 @@ export function resolveWorkspaceHandoffIdentity(
 export function createBetterAuthInstance(db: Db, config: Config, trustedOrigins: string[]): BetterAuthInstance {
   const baseUrl = config.authBaseUrlMode === "explicit" ? config.authPublicBaseUrl : undefined;
   const publicUrl = process.env.PAPERCLIP_PUBLIC_URL?.trim() || baseUrl;
+  const managedRuntimePublicUrl = process.env.PAPERCLIP_MANAGED_RUNTIME_PUBLIC_URL?.trim() || undefined;
   const secret = process.env.BETTER_AUTH_SECRET ?? process.env.PAPERCLIP_AGENT_JWT_SECRET;
   if (!secret) {
     throw new Error(
@@ -252,7 +309,48 @@ export function createBetterAuthInstance(db: Db, config: Config, trustedOrigins:
     delete (authConfig as { baseURL?: string }).baseURL;
   }
 
-  return betterAuth(authConfig);
+  const defaultAuth = betterAuth(authConfig);
+  const supportsManagedLoopbackAuth = Boolean(
+    !disableSecureCookies &&
+    isHttpsUrl(publicUrl) &&
+    isHttpsUrl(managedRuntimePublicUrl),
+  );
+  if (!supportsManagedLoopbackAuth) return defaultAuth;
+
+  // Better Auth fixes both the Secure attribute and the __Secure- name prefix
+  // when an instance is created. Keep the public instance unchanged and route
+  // only managed HTTP-loopback requests through a cookie-compatible instance.
+  const loopbackAuth = betterAuth({
+    ...authConfig,
+    advanced: buildBetterAuthAdvancedOptions({ disableSecureCookies: true }),
+  });
+  const cookieSecurityInput = {
+    deploymentMode: config.deploymentMode,
+    deploymentExposure: config.deploymentExposure,
+    authBaseUrlMode: config.authBaseUrlMode,
+    authPublicBaseUrl: config.authPublicBaseUrl,
+    publicUrl,
+    managedRuntimePublicUrl,
+  };
+
+  return {
+    handler: (request) => {
+      const auth = shouldDisableSecureAuthCookies({
+        ...cookieSecurityInput,
+        requestUrl: request.url,
+      }) ? loopbackAuth : defaultAuth;
+      return auth.handler(request);
+    },
+    api: {
+      getSession: (input) => {
+        const auth = shouldDisableSecureAuthCookies({
+          ...cookieSecurityInput,
+          requestUrl: requestUrlFromHeaders(input.headers),
+        }) ? loopbackAuth : defaultAuth;
+        return auth.api.getSession(input);
+      },
+    },
+  };
 }
 
 export function createBetterAuthHandler(auth: BetterAuthHandlerTarget): RequestHandler {