diff --git a/.github/workflows/e2e.yml b/.github/workflows/e2e.yml
index e000cdab4ba..2b5f939b20a 100644
--- a/.github/workflows/e2e.yml
+++ b/.github/workflows/e2e.yml
@@ -229,6 +229,7 @@ jobs:
             . != "tests/e2e/paired-startup-exec-readiness.spec.ts" and
             . != "tests/e2e/local-ssh-browser-routing.spec.ts" and
             . != "tests/e2e/ssh-browser-network-execution-route.docker.unit.test.ts" and
+            . != "tests/e2e/ssh-localhost.spec.ts" and
             . != "tests/e2e/ssh-client-hosted-browser-drop-reconnect.spec.ts" and
             . != "tests/e2e/ssh-docker-bulk-open-freeze-repro.spec.ts" and
             . != "tests/e2e/terminal-ibus-hangul-native.spec.ts"
@@ -375,3 +376,65 @@ jobs:
           ORCA_BACKGROUND_LAUNCH: '1'
           ORCA_RUN_DOCKER_SSH_BROWSER_E2E: '1'
         run: node_modules/.bin/vitest run --config config/vitest.config.ts tests/e2e/ssh-browser-network-execution-route.docker.unit.test.ts
+
+  ssh-localhost:
+    name: localhost SSH terminal and hooks
+    needs: [build, prepare-native-cache]
+    if: inputs.test_files == '' || contains(inputs.test_files, 'tests/e2e/ssh-localhost.spec.ts')
+    runs-on: ubuntu-latest
+    timeout-minutes: 20
+    steps:
+      - uses: actions/checkout@v6
+        with:
+          ref: ${{ inputs.ref || github.ref }}
+      - name: Install SSH server and headless tools
+        run: sudo apt-get update && sudo apt-get install -y build-essential openssh-client openssh-server python3 ripgrep xvfb zsh openbox x11-utils
+      - uses: ./.github/actions/install-node-dependencies
+        with:
+          native-runtime: electron
+      - uses: actions/download-artifact@v8
+        with:
+          name: e2e-build-out
+          path: out/
+      - name: Start isolated localhost SSH server
+        shell: bash
+        run: |
+          # Bare shells install Pi extensions only for an existing agent home.
+          mkdir -p "$HOME/.pi/agent"
+          fixture="$RUNNER_TEMP/orca-localhost-sshd"
+          mkdir -p "$fixture"
+          ssh-keygen -q -t ed25519 -N '' -f "$fixture/host_key"
+          ssh-keygen -q -t ed25519 -N '' -f "$fixture/client_key"
+          cat > "$fixture/sshd_config" <<EOF
+          Port 22222
+          ListenAddress 127.0.0.1
+          HostKey $fixture/host_key
+          PidFile $fixture/sshd.pid
+          AuthorizedKeysFile $fixture/client_key.pub
+          StrictModes no
+          PasswordAuthentication no
+          KbdInteractiveAuthentication no
+          UsePAM yes
+          AllowUsers $(id -un)
+          Subsystem sftp internal-sftp
+          EOF
+          sudo mkdir -p /run/sshd
+          sudo /usr/sbin/sshd -f "$fixture/sshd_config" -E "$fixture/sshd.log"
+          ssh -i "$fixture/client_key" -p 22222 -o BatchMode=yes -o StrictHostKeyChecking=no -o UserKnownHostsFile=/dev/null 127.0.0.1 true || { sudo cat "$fixture/sshd.log"; exit 1; }
+          echo "ORCA_E2E_SSH_PORT=22222" >> "$GITHUB_ENV"
+          echo "ORCA_E2E_SSH_USER=$(id -un)" >> "$GITHUB_ENV"
+          echo "ORCA_E2E_SSH_IDENTITY_FILE=$fixture/client_key" >> "$GITHUB_ENV"
+      - name: Run localhost SSH terminal and hook journey
+        env:
+          SKIP_BUILD: '1'
+          ORCA_E2E_SSH_LOCALHOST: '1'
+          ORCA_FEATURE_REMOTE_AGENT_HOOKS: '1'
+          ORCA_E2E_FORWARD_APP_LOGS: '1'
+        run: xvfb-run --auto-servernum bash .github/scripts/e2e-with-window-manager.sh pnpm exec playwright test --config tests/playwright.config.ts tests/e2e/ssh-localhost.spec.ts --project=electron-headless --workers=1
+      - uses: actions/upload-artifact@v7
+        if: failure()
+        with:
+          name: localhost-ssh-traces
+          path: test-results/
+          retention-days: 7
+          if-no-files-found: ignore
diff --git a/config/scripts/release-cut-token-permissions.test.mjs b/config/scripts/release-cut-token-permissions.test.mjs
index 85f36dea3a0..0fc1e5f8448 100644
--- a/config/scripts/release-cut-token-permissions.test.mjs
+++ b/config/scripts/release-cut-token-permissions.test.mjs
@@ -13,6 +13,7 @@ const EXPECTED_MATRIX = {
   '.github/workflows/e2e.yml#e2e': { contents: 'read' },
   '.github/workflows/e2e.yml#prepare-native-cache': { contents: 'read' },
   '.github/workflows/e2e.yml#ssh-browser-network-route': { contents: 'read' },
+  '.github/workflows/e2e.yml#ssh-localhost': { contents: 'read' },
   '.github/workflows/e2e.yml#ssh-docker-watcher-isolation': { contents: 'read' },
   '.github/workflows/homebrew-bump.yml#bump-cask': { contents: 'read' },
   '.github/workflows/release-mac-build.yml#build-mac': { contents: 'write' },
diff --git a/config/scripts/run-ssh-docker-e2e.mjs b/config/scripts/run-ssh-docker-e2e.mjs
index 4b9d51137f1..b88bde609bb 100644
--- a/config/scripts/run-ssh-docker-e2e.mjs
+++ b/config/scripts/run-ssh-docker-e2e.mjs
@@ -48,10 +48,9 @@ if (runtime.status !== 0) {
 //   - E2E does not gate merges: `verify.needs` in pr.yml omits `e2e` while the suite is red on
 //     main. Nothing in this lane blocks a PR yet. pr.yml's Require-successful-checks comment
 //     has the exact wiring to flip it, and the gate contract asserts the current state.
-//   - Three specs are gated on env vars no workflow sets, so they run nowhere
+//   - Two specs are gated on env vars no workflow sets, so they run nowhere
 //     and are not Docker-gated, which puts them outside this file's contract:
 //       nested-runtime-ssh-lifecycle, nested-runtime-ssh-routing (ORCA_E2E_NESTED_RUNTIME_SSH)
-//       ssh-localhost (ORCA_E2E_SSH_LOCALHOST)
 //     The nested-runtime runner remains unused by CI.
 const result = spawnSync(
   pnpm,
diff --git a/config/scripts/ssh-localhost-e2e-routing.test.mjs b/config/scripts/ssh-localhost-e2e-routing.test.mjs
new file mode 100644
index 00000000000..abab627dfb5
--- /dev/null
+++ b/config/scripts/ssh-localhost-e2e-routing.test.mjs
@@ -0,0 +1,35 @@
+import { readFileSync } from 'node:fs'
+import { resolve } from 'node:path'
+import { parse } from 'yaml'
+import { expect, it } from 'vitest'
+
+const workflow = parse(
+  readFileSync(resolve(import.meta.dirname, '../../.github/workflows/e2e.yml'), 'utf8')
+)
+
+it('gives the localhost SSH journey its same-filesystem server and agent prerequisite', () => {
+  const spec = 'tests/e2e/ssh-localhost.spec.ts'
+  const job = workflow.jobs['ssh-localhost']
+  expect(job.if).toContain("inputs.test_files == ''")
+  expect(job.if).toContain(spec)
+  expect(job['runs-on']).toBe('ubuntu-latest')
+  expect(job.needs).toEqual(['build', 'prepare-native-cache'])
+  const setup = job.steps.find((step) => step.name === 'Start isolated localhost SSH server')
+  expect(setup.run).toContain('ListenAddress 127.0.0.1')
+  expect(setup.run).toContain('PasswordAuthentication no')
+  expect(setup.run).toContain('UsePAM yes')
+  expect(setup.run).toContain('mkdir -p "$HOME/.pi/agent"')
+  for (const key of ['ORCA_E2E_SSH_PORT', 'ORCA_E2E_SSH_USER', 'ORCA_E2E_SSH_IDENTITY_FILE']) {
+    expect(setup.run).toContain(key)
+  }
+  const run = job.steps.find((step) => step.name === 'Run localhost SSH terminal and hook journey')
+  expect(run.env.ORCA_E2E_SSH_LOCALHOST).toBe('1')
+  expect(run.env.ORCA_FEATURE_REMOTE_AGENT_HOOKS).toBe('1')
+  expect(run.run).toContain(spec)
+  expect(run.run).toContain('--project=electron-headless')
+  expect(run.run).not.toContain('--retries')
+  expect(run['continue-on-error']).toBeUndefined()
+  expect(
+    workflow.jobs['changed-e2e'].steps.find((step) => step.name === 'Run changed E2E specs').run
+  ).toContain(`. != "${spec}"`)
+})