diff --git a/neonvm-controller/cmd/main.go b/neonvm-controller/cmd/main.go
index fb8046f85..c56eb6db8 100644
--- a/neonvm-controller/cmd/main.go
+++ b/neonvm-controller/cmd/main.go
@@ -100,6 +100,7 @@ func main() {
 	var memhpAutoMovableRatio string
 	var failurePendingPeriod time.Duration
 	var failingRefreshInterval time.Duration
+	var atMostOnePod bool
 	flag.StringVar(&metricsAddr, "metrics-bind-address", ":8080", "The address the metric endpoint binds to.")
 	flag.StringVar(&probeAddr, "health-probe-bind-address", ":8081", "The address the probe endpoint binds to.")
 	flag.BoolVar(&enableLeaderElection, "leader-elect", false,
@@ -140,6 +141,9 @@ func main() {
 		"the period for the propagation of reconciliation failures to the observability instruments")
 	flag.DurationVar(&failingRefreshInterval, "failing-refresh-interval", 1*time.Minute,
 		"the interval between consecutive updates of metrics and logs, related to failing reconciliations")
+	flag.BoolVar(&atMostOnePod, "at-most-one-pod", false,
+		"If true, the controller will ensure that at most one pod is running at a time. "+
+			"Otherwise, the outdated pod might be left to terminate, while the new one is already running.")
 	flag.Parse()
 
 	if defaultMemoryProvider == "" {
@@ -195,6 +199,7 @@ func main() {
 		MemhpAutoMovableRatio:   memhpAutoMovableRatio,
 		FailurePendingPeriod:    failurePendingPeriod,
 		FailingRefreshInterval:  failingRefreshInterval,
+		AtMostOnePod:            atMostOnePod,
 	}
 
 	vmReconciler := &controllers.VMReconciler{
diff --git a/pkg/neonvm/controllers/config.go b/pkg/neonvm/controllers/config.go
index eb81d98b2..69616e73d 100644
--- a/pkg/neonvm/controllers/config.go
+++ b/pkg/neonvm/controllers/config.go
@@ -50,4 +50,7 @@ type ReconcilerConfig struct {
 	// FailingRefreshInterval is the interval between consecutive
 	// updates of metrics and logs, related to failing reconciliations
 	FailingRefreshInterval time.Duration
+
+	// AtMostOnePod is the flag that indicates whether we should only have one pod per VM.
+	AtMostOnePod bool
 }
diff --git a/pkg/neonvm/controllers/functests/vm_controller_test.go b/pkg/neonvm/controllers/functests/vm_controller_test.go
index 542dcb88b..8b3987b6c 100644
--- a/pkg/neonvm/controllers/functests/vm_controller_test.go
+++ b/pkg/neonvm/controllers/functests/vm_controller_test.go
@@ -115,6 +115,7 @@ var _ = Describe("VirtualMachine controller", func() {
 					MemhpAutoMovableRatio:   "301",
 					FailurePendingPeriod:    1 * time.Minute,
 					FailingRefreshInterval:  1 * time.Minute,
+					AtMostOnePod:            false,
 				},
 			}
 
diff --git a/pkg/neonvm/controllers/vm_controller.go b/pkg/neonvm/controllers/vm_controller.go
index 338991bb2..d06bf5f1f 100644
--- a/pkg/neonvm/controllers/vm_controller.go
+++ b/pkg/neonvm/controllers/vm_controller.go
@@ -772,13 +772,12 @@ func (r *VMReconciler) doReconcile(ctx context.Context, vm *vmv1.VirtualMachine)
 			return err
 		}
 
-		// We must keep the VM status the same until we know the neonvm-runner container has been
-		// terminated, otherwise we could end up starting a new runner pod while the VM in the old
-		// one is still running.
+		// By default, we cleanup the VM, even if previous pod still exists. This behavior is for the case
+		// where the pod is stuck deleting, and we want to progress without waiting for it.
 		//
-		// Note that this is required because 'VmSucceeded' and 'VmFailed' are true if *at least
-		// one* container inside the runner pod has finished; the VM itself may still be running.
-		if apierrors.IsNotFound(err) || runnerContainerStopped(vmRunner) {
+		// However, this opens up a possibility for cascading failures where the pods would be constantly
+		// recreated, and then stuck deleting. That's why we have AtMostOnePod.
+		if !r.Config.AtMostOnePod || apierrors.IsNotFound(err) {
 			// NB: Cleanup() leaves status .Phase and .RestartCount (+ some others) but unsets other fields.
 			vm.Cleanup()
 
@@ -957,23 +956,6 @@ func runnerStatus(pod *corev1.Pod) runnerStatusKind {
 	}
 }
 
-// runnerContainerStopped returns true iff the neonvm-runner container has exited.
-//
-// The guarantee is simple: It is only safe to start a new runner pod for a VM if
-// runnerContainerStopped returns true (otherwise, we may end up with >1 instance of the same VM).
-func runnerContainerStopped(pod *corev1.Pod) bool {
-	if pod.Status.Phase == corev1.PodSucceeded || pod.Status.Phase == corev1.PodFailed {
-		return true
-	}
-
-	for _, stat := range pod.Status.ContainerStatuses {
-		if stat.Name == "neonvm-runner" {
-			return stat.State.Terminated != nil
-		}
-	}
-	return false
-}
-
 // deleteRunnerPodIfEnabled deletes the runner pod if buildtag.NeverDeleteRunnerPods is false, and
 // then emits an event and log line about what it did, whether it actually deleted the runner pod.
 func (r *VMReconciler) deleteRunnerPodIfEnabled(
diff --git a/pkg/neonvm/controllers/vm_controller_unit_test.go b/pkg/neonvm/controllers/vm_controller_unit_test.go
index 139252924..f77d8d1a2 100644
--- a/pkg/neonvm/controllers/vm_controller_unit_test.go
+++ b/pkg/neonvm/controllers/vm_controller_unit_test.go
@@ -123,6 +123,7 @@ func newTestParams(t *testing.T) *testParams {
 			MemhpAutoMovableRatio:   "301",
 			FailurePendingPeriod:    time.Minute,
 			FailingRefreshInterval:  time.Minute,
+			AtMostOnePod:            false,
 		},
 		Metrics: reconcilerMetrics,
 	}