diff --git a/.github/workflows/e2e-test.yml b/.github/workflows/e2e-test.yml
index ea870d98e..cb7bc67d1 100644
--- a/.github/workflows/e2e-test.yml
+++ b/.github/workflows/e2e-test.yml
@@ -205,3 +205,67 @@ jobs:
       - name: Print AppArmor denials
         if: always()
         run: sudo dmesg | grep -E 'apparmor=.*DENIED|profile="unprivileged_userns"' | tail -100 || true
+
+  e2e-vm:
+    name: E2E (rust-vm)
+    # libkrun needs KVM, so this job must run directly on a GitHub-hosted
+    # Linux VM. GitHub-hosted macOS runners do not support nested
+    # virtualization, and a job container would hide the host KVM device.
+    runs-on: ubuntu-24.04
+    timeout-minutes: 90
+    env:
+      GH_TOKEN: ${{ secrets.GITHUB_TOKEN }}
+      MISE_GITHUB_TOKEN: ${{ secrets.GITHUB_TOKEN }}
+    steps:
+      - uses: actions/checkout@9c091bb21b7c1c1d1991bb908d89e4e9dddfe3e0 # v7.0.0
+        with:
+          ref: ${{ inputs['checkout-ref'] || github.sha }}
+          persist-credentials: false
+
+      - name: Enable KVM access
+        run: |
+          set -euo pipefail
+          if [[ ! -c /dev/kvm ]]; then
+            echo "::error::The GitHub-hosted runner did not expose /dev/kvm"
+            lscpu
+            grep -m1 -E '^(flags|Features)' /proc/cpuinfo || true
+            ls -la /dev
+            exit 1
+          fi
+          sudo chmod 0666 /dev/kvm
+          ls -l /dev/kvm
+          test -r /dev/kvm
+          test -w /dev/kvm
+
+      - name: Install system dependencies
+        run: |
+          sudo apt-get update
+          sudo apt-get install -y --no-install-recommends \
+            build-essential \
+            clang \
+            cmake \
+            libclang-dev \
+            libssl-dev \
+            libz3-dev \
+            openssh-client \
+            pkg-config \
+            socat \
+            zstd
+
+      - name: Install mise
+        run: |
+          curl https://mise.run | MISE_VERSION=v2026.4.25 sh
+          echo "$HOME/.local/bin" >> "$GITHUB_PATH"
+          echo "$HOME/.local/share/mise/shims" >> "$GITHUB_PATH"
+
+      - name: Install tools
+        run: mise install --locked
+
+      - name: Cache Rust target and registry
+        uses: Swatinem/rust-cache@c19371144df3bb44fab255c43d04cbc2ab54d1c4 # v2
+        with:
+          shared-key: e2e-vm-linux-amd64
+          cache-on-failure: "true"
+
+      - name: Run VM E2E
+        run: mise run --no-deps --skip-deps e2e:vm
diff --git a/CI.md b/CI.md
index e14d5bdb9..19fad7bd3 100644
--- a/CI.md
+++ b/CI.md
@@ -14,7 +14,8 @@ Merge queue validation is a second integration gate for `main`. After a PR has p
 
 Three opt-in labels enable the long-running E2E suites:
 
-- `test:e2e` runs the standard E2E suite in `Branch E2E Checks`
+- `test:e2e` runs the standard Docker, rootless Podman, Kubernetes, and VM E2E
+  suites in `Branch E2E Checks`
 - `test:e2e-gpu` runs GPU E2E in `Branch E2E Checks`
 - `test:e2e-kubernetes` runs Kubernetes E2E with the HA Helm overlay
   (`replicaCount: 2` and bundled PostgreSQL) in `Branch E2E Checks`
diff --git a/TESTING.md b/TESTING.md
index d32dc385c..a032baa5e 100644
--- a/TESTING.md
+++ b/TESTING.md
@@ -150,6 +150,7 @@ Suites:
 - Common suite (`--features e2e`) - driver-neutral CLI behavior, sandbox lifecycle, sync, port forwarding, policy, and provider tests.
 - Docker suite (`--features e2e-docker`) - common suite plus Docker-only coverage such as Dockerfile image builds, Docker preflight checks, and managed Docker gateway resume.
 - Docker GPU suite (`--features e2e-docker-gpu`) - Docker suite plus GPU sandbox smoke coverage.
+- VM suite (`--features e2e-vm`) - runs e2e tests on a VM.
 
 GPU device-selection tests compare OpenShell sandboxes against a plain Docker or
 Podman container that requests `--device nvidia.com/gpu=all`. The probe image
@@ -173,6 +174,12 @@ Run the Podman-backed Rust CLI e2e suite:
 mise run e2e:podman
 ```
 
+Run the VM-backed Rust CLI e2e suite:
+
+```shell
+mise run e2e:vm
+```
+
 Run a single test directly with cargo:
 
 ```shell
diff --git a/architecture/build.md b/architecture/build.md
index e3ac5012e..63d4e5684 100644
--- a/architecture/build.md
+++ b/architecture/build.md
@@ -148,7 +148,8 @@ The high-level CI model:
 
 1. PR-context gate jobs publish required statuses for the PR head commit.
 2. Standard branch checks run from trusted mirror branches.
-3. Label-gated E2E, GPU, and Kubernetes checks run from trusted mirror branches.
+3. Label-gated Docker, Podman, VM, GPU, and Kubernetes E2E checks run from
+   trusted mirror branches.
 4. Merge-group checks run against GitHub's temporary queue branch for the final integration state.
 5. Gate jobs verify that the mirror branch matches the PR head, or that the merge-group workflow ran for the queued SHA, and that the expected non-gate workflow actually ran.
 6. Release workflows rebuild and publish binaries, wheels, images, and docs.
diff --git a/e2e/rust/e2e-vm.sh b/e2e/rust/e2e-vm.sh
index ef798a8ea..8005d09bd 100755
--- a/e2e/rust/e2e-vm.sh
+++ b/e2e/rust/e2e-vm.sh
@@ -315,4 +315,5 @@ if [ -n "${E2E_TEST_OVERRIDE}" ]; then
 else
   run_e2e_test smoke
   run_e2e_test host_gateway_alias
+  run_e2e_test vm_gateway_resume
 fi
diff --git a/e2e/rust/tests/vm_gateway_resume.rs b/e2e/rust/tests/vm_gateway_resume.rs
index b2ec6c8b5..4c502bb9c 100644
--- a/e2e/rust/tests/vm_gateway_resume.rs
+++ b/e2e/rust/tests/vm_gateway_resume.rs
@@ -36,8 +36,11 @@ async fn vm_gateway_restart_resumes_running_sandbox() {
         .await
         .expect("gateway should start healthy");
 
+    // The gateway restart terminates the VM process before re-adopting its
+    // overlay. Flush the marker before reporting readiness so the assertion
+    // verifies durable overlay state rather than guest page-cache timing.
     let script = format!(
-        "echo before-restart > {RESUME_FILE}; echo {READY_MARKER}; while true; do sleep 1; done"
+        "echo before-restart > {RESUME_FILE}; sync; echo {READY_MARKER}; while true; do sleep 1; done"
     );
     let mut sandbox = SandboxGuard::create_keep(&["sh", "-lc", &script], READY_MARKER)
         .await