diff --git a/src/lib/actions/sandbox/connect.ts b/src/lib/actions/sandbox/connect.ts
index 689d7d22278..3d7cac3e955 100644
--- a/src/lib/actions/sandbox/connect.ts
+++ b/src/lib/actions/sandbox/connect.ts
@@ -85,11 +85,12 @@ import {
   type GatewayRestartFailureLayer,
   type ManagedGatewayControlCompletion,
   resolveSandboxDashboardPort,
+  waitForManagedGatewaySupervisor,
 } from "./process-recovery";
 import { runTerminalAgentConnectProbe } from "./terminal-connect-probe";
 import { applyOpenShellVmDnsMonkeypatch, shouldApplyVmDnsMonkeypatch } from "./vm-dns-monkeypatch";
 
-export { runConnectAutoPairApprovalPass };
+export { runConnectAutoPairApprovalPass, waitForManagedGatewaySupervisor };
 
 export type SandboxConnectOptions = {
   probeOnly?: boolean;
diff --git a/src/lib/actions/sandbox/start.test.ts b/src/lib/actions/sandbox/start.test.ts
index 2037a957c3e..3d984c1f0d3 100644
--- a/src/lib/actions/sandbox/start.test.ts
+++ b/src/lib/actions/sandbox/start.test.ts
@@ -58,6 +58,9 @@ function harness(overrides: Partial<SandboxStartDeps> = {}) {
   const restoreStartupState = vi.fn<NonNullable<SandboxStartDeps["restoreStartupState"]>>(
     () => SUCCESSFUL_RECOVERY,
   );
+  const waitForManagedGatewaySupervisor = vi.fn<
+    NonNullable<SandboxStartDeps["waitForManagedGatewaySupervisor"]>
+  >(() => false);
   const log = vi.fn<(message: string) => void>();
   const runtimeProviders = createRuntimeProviderBundleRegistry([
     [
@@ -76,6 +79,7 @@ function harness(overrides: Partial<SandboxStartDeps> = {}) {
     getSandbox,
     runtimeProviders,
     restoreStartupState,
+    waitForManagedGatewaySupervisor,
     verifyGateway,
     log,
     ...overrides,
@@ -90,6 +94,7 @@ function harness(overrides: Partial<SandboxStartDeps> = {}) {
     printDockerRuntimeDownGuidance,
     recoverDockerDriverSandbox,
     restoreStartupState,
+    waitForManagedGatewaySupervisor,
     verifyGateway,
   };
 }
@@ -164,6 +169,125 @@ describe("startSandbox", () => {
     );
   });
 
+  it("waits for a transient managed supervisor before repeating full startup recovery (#8726)", async () => {
+    const h = harness();
+    h.restoreStartupState
+      .mockReturnValueOnce({
+        ...FAILED_RECOVERY,
+        recoveryFailureLayer: "supervisor not running",
+        recoveryFailureDetail: "SUPERVISOR_NOT_RUNNING",
+      })
+      .mockReturnValueOnce(SUCCESSFUL_RECOVERY);
+    h.waitForManagedGatewaySupervisor.mockReturnValue(true);
+
+    const result = await startSandbox("my-sandbox", h.deps);
+
+    expect(result.exitCode).toBe(0);
+    expect(h.restoreStartupState).toHaveBeenCalledTimes(2);
+    expect(h.waitForManagedGatewaySupervisor).toHaveBeenCalledOnce();
+    expect(h.waitForManagedGatewaySupervisor).toHaveBeenCalledWith("my-sandbox");
+    expect(h.verifyGateway).toHaveBeenCalledOnce();
+    expect(h.restoreStartupState.mock.invocationCallOrder[0]).toBeLessThan(
+      h.waitForManagedGatewaySupervisor.mock.invocationCallOrder[0],
+    );
+    expect(h.waitForManagedGatewaySupervisor.mock.invocationCallOrder[0]).toBeLessThan(
+      h.restoreStartupState.mock.invocationCallOrder[1],
+    );
+    expect(h.restoreStartupState.mock.invocationCallOrder[1]).toBeLessThan(
+      h.verifyGateway.mock.invocationCallOrder[0],
+    );
+  });
+
+  it("preserves the first recovery failure when the managed supervisor remains absent (#8726)", async () => {
+    const h = harness();
+    h.restoreStartupState.mockReturnValue({
+      ...FAILED_RECOVERY,
+      recoveryFailureLayer: "supervisor not running",
+      recoveryFailureDetail: "SUPERVISOR_NOT_RUNNING",
+    });
+
+    await expect(startSandbox("my-sandbox", h.deps)).rejects.toThrow(
+      "supervisor not running: SUPERVISOR_NOT_RUNNING",
+    );
+    expect(h.restoreStartupState).toHaveBeenCalledOnce();
+    expect(h.waitForManagedGatewaySupervisor).toHaveBeenCalledOnce();
+    expect(h.verifyGateway).not.toHaveBeenCalled();
+  });
+
+  it("preserves the first recovery failure when the managed supervisor wait throws (#8726)", async () => {
+    const h = harness();
+    h.restoreStartupState.mockReturnValue({
+      ...FAILED_RECOVERY,
+      recoveryFailureLayer: "supervisor not running",
+      recoveryFailureDetail: "SUPERVISOR_NOT_RUNNING",
+    });
+    h.waitForManagedGatewaySupervisor.mockImplementation(() => {
+      throw new Error("managed supervisor probe failed");
+    });
+
+    await expect(startSandbox("my-sandbox", h.deps)).rejects.toThrow(
+      "supervisor not running: SUPERVISOR_NOT_RUNNING",
+    );
+    expect(h.restoreStartupState).toHaveBeenCalledOnce();
+    expect(h.waitForManagedGatewaySupervisor).toHaveBeenCalledOnce();
+    expect(h.verifyGateway).not.toHaveBeenCalled();
+  });
+
+  it("fails closed when recovery still fails after the managed supervisor appears (#8726)", async () => {
+    const h = harness();
+    const missingSupervisor = {
+      ...FAILED_RECOVERY,
+      recoveryFailureLayer: "supervisor not running" as const,
+      recoveryFailureDetail: "SUPERVISOR_NOT_RUNNING",
+    };
+    h.restoreStartupState.mockReturnValue(missingSupervisor);
+    h.waitForManagedGatewaySupervisor.mockReturnValue(true);
+
+    await expect(startSandbox("my-sandbox", h.deps)).rejects.toThrow(
+      "supervisor not running: SUPERVISOR_NOT_RUNNING",
+    );
+    expect(h.restoreStartupState).toHaveBeenCalledTimes(2);
+    expect(h.waitForManagedGatewaySupervisor).toHaveBeenCalledOnce();
+    expect(h.verifyGateway).not.toHaveBeenCalled();
+  });
+
+  it.each([
+    ["definitive supervisor failure", "supervisor unavailable", "SUPERVISOR_UNAVAILABLE"],
+    [
+      "unclassified missing-supervisor output",
+      "supervisor not running",
+      "prefix SUPERVISOR_NOT_RUNNING suffix",
+    ],
+  ] as const)("does not wait after a %s (#8726)", async (_label, layer, detail) => {
+    const h = harness();
+    h.restoreStartupState.mockReturnValue({
+      ...FAILED_RECOVERY,
+      recoveryFailureLayer: layer,
+      recoveryFailureDetail: detail,
+    });
+
+    await expect(startSandbox("my-sandbox", h.deps)).rejects.toThrow(detail);
+    expect(h.restoreStartupState).toHaveBeenCalledOnce();
+    expect(h.waitForManagedGatewaySupervisor).not.toHaveBeenCalled();
+    expect(h.verifyGateway).not.toHaveBeenCalled();
+  });
+
+  it("keeps successful legacy supervisor relaunch recovery free of a settling wait (#8726)", async () => {
+    const h = harness();
+    h.restoreStartupState.mockReturnValue({
+      ...SUCCESSFUL_RECOVERY,
+      wasRunning: false,
+      recovered: true,
+    });
+
+    const result = await startSandbox("my-sandbox", h.deps);
+
+    expect(result.exitCode).toBe(0);
+    expect(h.restoreStartupState).toHaveBeenCalledOnce();
+    expect(h.waitForManagedGatewaySupervisor).not.toHaveBeenCalled();
+    expect(h.verifyGateway).toHaveBeenCalledOnce();
+  });
+
   it.each([
     [
       "openclaw",
diff --git a/src/lib/actions/sandbox/start.ts b/src/lib/actions/sandbox/start.ts
index aeb74de90b6..1a197771925 100644
--- a/src/lib/actions/sandbox/start.ts
+++ b/src/lib/actions/sandbox/start.ts
@@ -54,10 +54,22 @@ export interface SandboxStartDeps {
   getSandbox?: typeof registry.getSandbox;
   runtimeProviders?: RuntimeProviderBundleRegistry;
   restoreStartupState?: (sandboxName: string) => SandboxStartupRecoveryResult;
+  waitForManagedGatewaySupervisor?: (sandboxName: string) => boolean;
   verifyGateway?: (sandboxName: string) => Promise<void>;
   log?: (message: string) => void;
 }
 
+function isMissingManagedSupervisorStartupFailure(
+  check: SandboxStartupRecoveryResult,
+  failure: string,
+): boolean {
+  return (
+    failure === "supervisor not running: SUPERVISOR_NOT_RUNNING" &&
+    check.recoveryFailureLayer === "supervisor not running" &&
+    check.recoveryFailureDetail === "SUPERVISOR_NOT_RUNNING"
+  );
+}
+
 function startupRecoveryFailure(check: SandboxStartupRecoveryResult): string | null {
   if (!check.checked) return "managed agent gateway inspection did not complete";
   if ("runtime" in check && check.runtime === "terminal") return null;
@@ -132,7 +144,27 @@ export async function startSandbox(
     } catch (error) {
       throw preservedSandboxRecoveryError(name, error);
     }
-    const failure = startupRecoveryFailure(recovery);
+    let failure = startupRecoveryFailure(recovery);
+    if (failure && isMissingManagedSupervisorStartupFailure(recovery, failure)) {
+      let supervisorReady = false;
+      try {
+        const waitForSupervisor =
+          deps.waitForManagedGatewaySupervisor ??
+          (require("./connect") as typeof import("./connect")).waitForManagedGatewaySupervisor;
+        supervisorReady = waitForSupervisor(name);
+      } catch {
+        // Preserve the authoritative first recovery failure when the bounded
+        // read-only settling probe itself cannot complete.
+      }
+      if (supervisorReady) {
+        try {
+          recovery = restoreStartupState(name);
+        } catch (error) {
+          throw preservedSandboxRecoveryError(name, error);
+        }
+        failure = startupRecoveryFailure(recovery);
+      }
+    }
     if (failure) throw preservedSandboxRecoveryError(name, failure);
     log("  Checking gateway health and host forwards…");
     await (deps.verifyGateway ?? verifyGateway)(name);