diff --git a/src/main/ssh/connection/ssh-connection-loopback-route.test.ts b/src/main/ssh/connection/ssh-connection-loopback-route.test.ts
new file mode 100644
index 00000000000..ab20392d642
--- /dev/null
+++ b/src/main/ssh/connection/ssh-connection-loopback-route.test.ts
@@ -0,0 +1,138 @@
+import { beforeEach, describe, expect, it, vi } from 'vitest'
+import { resetSshConnectionMocks } from './ssh-connection-test-harness'
+import { createCallbacks, createTarget } from './ssh-connection-test-fixtures'
+import { SshConnection } from './ssh-connection'
+import type { SystemSshLoopbackRoute } from '../system-transport/system-ssh-loopback-route'
+
+const { startRouteMock } = vi.hoisted(() => ({ startRouteMock: vi.fn() }))
+
+vi.mock('ssh2', async () =>
+  (await import('../__tests__/ssh-connection-test-client')).createSsh2Module()
+)
+vi.mock('../system-transport/system-ssh-binary', async () =>
+  (await import('./ssh-connection-test-harness')).createSystemSshBinaryModule()
+)
+vi.mock('../system-transport/system-ssh-args', async (importOriginal) =>
+  (await import('./ssh-connection-test-harness')).withSystemSshArgsMocks(await importOriginal())
+)
+vi.mock('../system-transport/system-ssh-command', async (importOriginal) =>
+  (await import('./ssh-connection-test-harness')).withSystemSshCommandMocks(await importOriginal())
+)
+vi.mock('../ssh-control-socket', async () =>
+  (await import('./ssh-connection-test-harness')).createControlSocketModule()
+)
+vi.mock('../config/ssh-config-parser', async () =>
+  (await import('./ssh-connection-test-harness')).createSshConfigParserModule()
+)
+vi.mock('../config/ssh-g-config-resolution', async (importOriginal) =>
+  (await import('./ssh-connection-test-harness')).withSshGConfigResolutionMocks(
+    await importOriginal()
+  )
+)
+// Why the gate is forced on: it is platform-gated to win32 and covered in its own suite; this suite is the lifecycle.
+vi.mock('../system-transport/system-ssh-loopback-route', () => ({
+  shouldUseSystemSshLoopbackRoute: () => true,
+  startSystemSshLoopbackRoute: startRouteMock
+}))
+
+function createRoute(localPort: number): SystemSshLoopbackRoute {
+  return {
+    args: { localPort, hostKeyAlias: 'example.com' },
+    onExit: vi.fn(),
+    dispose: vi.fn()
+  }
+}
+
+function deferRouteStart(): (route: SystemSshLoopbackRoute) => void {
+  let resolveRoute: (route: SystemSshLoopbackRoute) => void = () => undefined
+  startRouteMock.mockImplementationOnce(
+    () =>
+      new Promise<SystemSshLoopbackRoute>((resolve) => {
+        resolveRoute = resolve
+      })
+  )
+  return (route) => resolveRoute(route)
+}
+
+describe('SshConnection loopback route', () => {
+  beforeEach(() => {
+    resetSshConnectionMocks()
+    startRouteMock.mockReset()
+  })
+
+  it('routes later commands through the route once it is proven', async () => {
+    const finishStart = deferRouteStart()
+    const conn = new SshConnection(
+      createTarget({ proxyCommand: 'ssh -W %h:%p bastion.example.com' }),
+      createCallbacks()
+    )
+
+    await conn.connect()
+    expect(conn.getSystemSshBuildArgsOptions().loopbackRoute).toBeUndefined()
+
+    finishStart(createRoute(50001))
+    await vi.waitFor(() =>
+      expect(conn.getSystemSshBuildArgsOptions().loopbackRoute).toEqual({
+        localPort: 50001,
+        hostKeyAlias: 'example.com'
+      })
+    )
+  })
+
+  it('still builds a route for a reconnect that superseded a start in flight', async () => {
+    const finishStaleStart = deferRouteStart()
+    const finishCurrentStart = deferRouteStart()
+    const conn = new SshConnection(
+      createTarget({ proxyCommand: 'ssh -W %h:%p bastion.example.com' }),
+      createCallbacks()
+    )
+    await conn.connect()
+
+    await conn.reconnect()
+    expect(conn.getState().status).toBe('connected')
+    expect(startRouteMock).toHaveBeenCalledTimes(2)
+
+    const stale = createRoute(50001)
+    finishStaleStart(stale)
+    await vi.waitFor(() => expect(stale.dispose).toHaveBeenCalled())
+    expect(conn.getSystemSshBuildArgsOptions().loopbackRoute).toBeUndefined()
+
+    finishCurrentStart(createRoute(50002))
+    await vi.waitFor(() =>
+      expect(conn.getSystemSshBuildArgsOptions().loopbackRoute?.localPort).toBe(50002)
+    )
+  })
+
+  it('drops the route when its forward exits, so commands fall back to the proxy', async () => {
+    const finishStart = deferRouteStart()
+    const conn = new SshConnection(
+      createTarget({ proxyCommand: 'ssh -W %h:%p bastion.example.com' }),
+      createCallbacks()
+    )
+    await conn.connect()
+    const route = createRoute(50001)
+    finishStart(route)
+    await vi.waitFor(() => expect(route.onExit).toHaveBeenCalled())
+
+    const onExit = vi.mocked(route.onExit).mock.calls[0]?.[0]
+    onExit?.()
+
+    expect(conn.getSystemSshBuildArgsOptions().loopbackRoute).toBeUndefined()
+  })
+
+  it('disposes the route on disconnect', async () => {
+    const finishStart = deferRouteStart()
+    const conn = new SshConnection(
+      createTarget({ proxyCommand: 'ssh -W %h:%p bastion.example.com' }),
+      createCallbacks()
+    )
+    await conn.connect()
+    const route = createRoute(50001)
+    finishStart(route)
+    await vi.waitFor(() => expect(conn.getSystemSshBuildArgsOptions().loopbackRoute).toBeDefined())
+
+    await conn.disconnect()
+
+    expect(route.dispose).toHaveBeenCalled()
+  })
+})
diff --git a/src/main/ssh/connection/ssh-connection.ts b/src/main/ssh/connection/ssh-connection.ts
index 6f4e7920d87..11d39f5a0b8 100644
--- a/src/main/ssh/connection/ssh-connection.ts
+++ b/src/main/ssh/connection/ssh-connection.ts
@@ -199,7 +199,7 @@ export class SshConnection {
   private systemSshControlMasterDisabledForSession = false
   private systemSshGssapiOnlyForSession = false
   private systemSshLoopbackRoute: SystemSshLoopbackRoute | null = null
-  private systemSshLoopbackRouteStarting = false
+  private systemSshLoopbackRouteStartingGeneration: number | null = null
   private useSystemSshTransport = false
   private credentialAbortController = new AbortController()
   private readonly pendingSsh2Clients = new Set<SshClient>()
@@ -1107,15 +1107,21 @@ export class SshConnection {
     const options = this.getSystemSshBuildArgsOptions()
     if (
       this.systemSshLoopbackRoute ||
-      this.systemSshLoopbackRouteStarting ||
+      this.systemSshLoopbackRouteStartingGeneration === connectGeneration ||
       !shouldUseSystemSshLoopbackRoute(this.target, this.systemSshResolvedConfig, options)
     ) {
       return
     }
-    this.systemSshLoopbackRouteStarting = true
+    // Why per generation: a start a reconnect superseded can still be in flight, and must not block the new one.
+    this.systemSshLoopbackRouteStartingGeneration = connectGeneration
+    const settle = (): void => {
+      if (this.systemSshLoopbackRouteStartingGeneration === connectGeneration) {
+        this.systemSshLoopbackRouteStartingGeneration = null
+      }
+    }
     startSystemSshLoopbackRoute(this.target, this.systemSshResolvedConfig, options).then(
       (route) => {
-        this.systemSshLoopbackRouteStarting = false
+        settle()
         if (!this.isCurrentConnectAttempt(connectGeneration) || !this.useSystemSshTransport) {
           route.dispose()
           return
@@ -1129,7 +1135,7 @@ export class SshConnection {
       },
       () => {
         // Why: per-command proxy logins still work; the route only makes them cheaper.
-        this.systemSshLoopbackRouteStarting = false
+        settle()
       }
     )
   }