diff --git a/doc/DEVELOPING.md b/doc/DEVELOPING.md
index b50fc3e7c69..62f1d90fbb1 100644
--- a/doc/DEVELOPING.md
+++ b/doc/DEVELOPING.md
@@ -892,6 +892,9 @@ Seed modes:
 The CLI and managed runtime provisioner honor it even when a registered source
 instance is present. An explicit successful `worktree reseed`, or a replacement
 `worktree init --force` without `--empty`, clears the choice.
+While that marker exists, startup uses the instance's saved JWT and tool-action
+signing keys even if the shell inherited another instance's keys. Better Auth
+uses its saved key or the fresh instance JWT key. Missing saved keys stop startup.
 
 Seeded worktree instances quarantine copied live execution by default for both `minimal` and `full` seeds. During restore, Paperclip disables copied agent timer heartbeats, resets copied `running` agents to `idle`, blocks and unassigns copied agent-owned `in_progress` issues, and unassigns copied agent-owned `todo`/`in_review` issues. This keeps a freshly booted worktree from starting agents for work already owned by the source instance. Pass `--preserve-live-work` only when you intentionally want the isolated worktree to resume copied assignments.
 
diff --git a/server/src/__tests__/dev-runner-worktree.test.ts b/server/src/__tests__/dev-runner-worktree.test.ts
index 5dd179edb58..786d8cd957f 100644
--- a/server/src/__tests__/dev-runner-worktree.test.ts
+++ b/server/src/__tests__/dev-runner-worktree.test.ts
@@ -4,6 +4,7 @@ import path from "node:path";
 import { afterEach, describe, expect, it } from "vitest";
 import {
   bootstrapDevRunnerWorktreeEnv,
+  applyEmptyWorktreeSigningSecrets,
   isWorktreeSeedPending,
   isLinkedGitWorktreeCheckout,
   resolveWorktreeEnvFilePath,
@@ -25,6 +26,18 @@ function createTempRoot(prefix: string): string {
 }
 
 describe("dev-runner worktree env bootstrap", () => {
+  it("uses saved empty-instance signing keys instead of inherited source keys", () => {
+    const root = createTempRoot("paperclip-empty-signing-keys-");
+    fs.mkdirSync(path.join(root, ".paperclip"));
+    fs.writeFileSync(path.join(root, ".git"), "gitdir: /tmp/paperclip/.git/worktrees/empty\n");
+    fs.writeFileSync(path.join(root, ".paperclip", "seed-empty"), "explicitly empty\n");
+    fs.writeFileSync(resolveWorktreeEnvFilePath(root), 'PAPERCLIP_AGENT_JWT_SECRET="fresh-jwt"\nPAPERCLIP_TOOL_ACTION_SIGNING_SECRET="fresh-actions"\n');
+    const env = { PAPERCLIP_AGENT_JWT_SECRET: "source-jwt", PAPERCLIP_TOOL_ACTION_SIGNING_SECRET: "source-actions", BETTER_AUTH_SECRET: "source-auth" };
+    bootstrapDevRunnerWorktreeEnv(root, env);
+    expect(env).toMatchObject({ PAPERCLIP_AGENT_JWT_SECRET: "fresh-jwt", PAPERCLIP_TOOL_ACTION_SIGNING_SECRET: "fresh-actions", BETTER_AUTH_SECRET: "fresh-jwt" });
+    fs.writeFileSync(resolveWorktreeEnvFilePath(root), 'PAPERCLIP_AGENT_JWT_SECRET="fresh-jwt"\n');
+    expect(() => applyEmptyWorktreeSigningSecrets(root, env)).toThrow("missing its saved PAPERCLIP_TOOL_ACTION_SIGNING_SECRET");
+  });
   it("guards seed-pending worktrees until a seed-complete marker exists", () => {
     const root = createTempRoot("paperclip-dev-runner-seed-pending-");
     fs.mkdirSync(path.join(root, ".paperclip"), { recursive: true });
diff --git a/server/src/__tests__/worktree-seed-server-spawn.test.ts b/server/src/__tests__/worktree-seed-server-spawn.test.ts
index 47710c59fb1..860dfffcab3 100644
--- a/server/src/__tests__/worktree-seed-server-spawn.test.ts
+++ b/server/src/__tests__/worktree-seed-server-spawn.test.ts
@@ -2,7 +2,7 @@ import { execFile } from "node:child_process";
 import fs from "node:fs/promises";
 import os from "node:os";
 import path from "node:path";
-import { fileURLToPath } from "node:url";
+import { fileURLToPath, pathToFileURL } from "node:url";
 import { promisify } from "node:util";
 import { afterEach, describe, expect, it, vi } from "vitest";
 import {
@@ -107,6 +107,24 @@ describe("managed worktree seed source through the server spawn path", () => {
       process.chdir(cwd);
       await worktreeInitCommand({ empty: true, fromConfig: sourceConfigPath, home: path.join(tempRoot, "instances") });
       const configPath = path.join(cwd, ".paperclip", "config.json");
+      const repoRoot = fileURLToPath(new URL("../../../", import.meta.url));
+      const startup = await execFileAsync(process.execPath, [path.join(repoRoot, "cli/node_modules/tsx/dist/cli.mjs"), "--eval", `
+        void (async () => {
+          const fs = await import('node:fs');
+          const dotenv = (await import(${JSON.stringify(pathToFileURL(path.join(repoRoot, "server/node_modules/dotenv/lib/main.js")).href)})).default;
+          const envPath = ${JSON.stringify(path.join(cwd, ".paperclip", ".env"))};
+          const saved = dotenv.parse(fs.readFileSync(envPath));
+          await import(${JSON.stringify(pathToFileURL(path.join(repoRoot, "server/src/config.ts")).href)});
+          const repaired = dotenv.parse(fs.readFileSync(envPath));
+          console.log(JSON.stringify({
+            jwt: process.env.PAPERCLIP_AGENT_JWT_SECRET === saved.PAPERCLIP_AGENT_JWT_SECRET,
+            actions: process.env.PAPERCLIP_TOOL_ACTION_SIGNING_SECRET === saved.PAPERCLIP_TOOL_ACTION_SIGNING_SECRET,
+            auth: process.env.BETTER_AUTH_SECRET === saved.PAPERCLIP_AGENT_JWT_SECRET,
+            savedActions: repaired.PAPERCLIP_TOOL_ACTION_SIGNING_SECRET === saved.PAPERCLIP_TOOL_ACTION_SIGNING_SECRET
+          }));
+        })();
+      `], { cwd, env: { ...process.env, PAPERCLIP_CONFIG: configPath, PAPERCLIP_AGENT_JWT_SECRET: "source-jwt", PAPERCLIP_TOOL_ACTION_SIGNING_SECRET: "source-actions", BETTER_AUTH_SECRET: "source-auth" } });
+      expect(JSON.parse(startup.stdout.trim().split("\n").at(-1)!)).toEqual({ jwt: true, actions: true, auth: true, savedActions: true });
       const workspace = {
         baseCwd, cwd, source: "project_primary" as const, projectId: "project-1",
         workspaceId: "project-workspace-1", repoUrl: null, repoRef: "HEAD",
diff --git a/server/src/config.ts b/server/src/config.ts
index 11de3894185..db5efb2cbda 100644
--- a/server/src/config.ts
+++ b/server/src/config.ts
@@ -2,11 +2,12 @@ import { readConfigFile, resolveDeploymentMode } from "./config-file.js";
 import { parseChatWebhookPublicBaseUrl } from "./chat-webhook-public-url.js";
 import { execFileSync } from "node:child_process";
 import { existsSync, realpathSync } from "node:fs";
-import { resolve } from "node:path";
+import { basename, dirname, resolve } from "node:path";
 import { config as loadDotenv } from "dotenv";
 import { resolvePaperclipEnvPath } from "./paths.js";
 import { maybeRepairLegacyWorktreeConfigAndEnvFiles } from "./worktree-config.js";
 import { shouldLoadWorkingDirectoryEnv } from "./env-file-policy.js";
+import { applyEmptyWorktreeSigningSecrets } from "./dev-runner-worktree.js";
 import {
   AUTH_BASE_URL_MODES,
   BIND_MODES,
@@ -48,6 +49,9 @@ if (shouldLoadWorkingDirectoryEnv({
   loadDotenv({ path: CWD_ENV_PATH, override: false, quiet: true });
 }
 
+if (basename(dirname(PAPERCLIP_ENV_FILE_PATH)) === ".paperclip") {
+  applyEmptyWorktreeSigningSecrets(dirname(dirname(PAPERCLIP_ENV_FILE_PATH)));
+}
 maybeRepairLegacyWorktreeConfigAndEnvFiles();
 
 const TAILSCALE_DETECT_TIMEOUT_MS = 3000;
diff --git a/server/src/dev-runner-worktree.ts b/server/src/dev-runner-worktree.ts
index b78e80fe70b..f28ddc06a88 100644
--- a/server/src/dev-runner-worktree.ts
+++ b/server/src/dev-runner-worktree.ts
@@ -57,6 +57,19 @@ export function resolveWorktreeEnvFilePath(rootDir: string): string {
   return path.resolve(rootDir, ".paperclip", ".env");
 }
 
+/** An explicitly empty instance owns its saved keys, even in an agent shell. */
+export function applyEmptyWorktreeSigningSecrets(rootDir: string, env: NodeJS.ProcessEnv = process.env): boolean {
+  if (!existsSync(path.resolve(rootDir, ".paperclip", "seed-empty"))) return false;
+  const entries = parseEnvFile(readFileSync(resolveWorktreeEnvFilePath(rootDir), "utf8"));
+  for (const key of ["PAPERCLIP_AGENT_JWT_SECRET", "PAPERCLIP_TOOL_ACTION_SIGNING_SECRET"] as const) {
+    if (!entries[key]?.trim()) throw new Error(`Empty worktree is missing its saved ${key}. Reinitialize its configuration before starting.`);
+    env[key] = entries[key];
+  }
+  // Better Auth otherwise prefers an inherited key over this instance's JWT key.
+  env.BETTER_AUTH_SECRET = entries.BETTER_AUTH_SECRET?.trim() || entries.PAPERCLIP_AGENT_JWT_SECRET;
+  return true;
+}
+
 export function isWorktreeSeedPending(rootDir: string): boolean {
   const markerDir = path.resolve(rootDir, ".paperclip");
   const manifestPath = path.resolve(markerDir, "seed-manifest.json");
@@ -134,6 +147,7 @@ export function bootstrapDevRunnerWorktreeEnv(
     if (typeof env[key] === "string" && env[key]!.trim().length > 0) continue;
     env[key] = value;
   }
+  applyEmptyWorktreeSigningSecrets(rootDir, env);
 
   return {
     envPath,
diff --git a/server/src/worktree-config.ts b/server/src/worktree-config.ts
index bd8d5d129d6..86ea6e1b258 100644
--- a/server/src/worktree-config.ts
+++ b/server/src/worktree-config.ts
@@ -16,6 +16,7 @@ import {
 } from "@paperclipai/shared/worktree-port-registry";
 import { resolvePaperclipConfigPath, resolvePaperclipEnvPath } from "./paths.js";
 import { rewriteUrlPort } from "./url-utils.js";
+import { applyEmptyWorktreeSigningSecrets } from "./dev-runner-worktree.js";
 
 function nonEmpty(value: string | null | undefined): string | null {
   return typeof value === "string" && value.trim().length > 0 ? value.trim() : null;
@@ -455,6 +456,8 @@ export function maybeRepairLegacyWorktreeConfigAndEnvFiles(): {
     return { repairedConfig: false, repairedEnv: false };
   }
 
+  applyEmptyWorktreeSigningSecrets(path.resolve(path.dirname(context.configPath), ".."));
+
   process.env.PAPERCLIP_HOME = context.homeDir;
   process.env.PAPERCLIP_INSTANCE_ID = context.instanceId;
   process.env.PAPERCLIP_CONFIG = context.configPath;