diff --git a/pkg/minikube/cruntime/crio.go b/pkg/minikube/cruntime/crio.go
index 4da2bf4bada3..258bdebb89cc 100644
--- a/pkg/minikube/cruntime/crio.go
+++ b/pkg/minikube/cruntime/crio.go
@@ -54,10 +54,9 @@ type CRIO struct {
 
 // generateCRIOConfig sets up /etc/crio/crio.conf
 func generateCRIOConfig(cr CommandRunner, imageRepository string, kv semver.Version) error {
-	cPath := crioConfigFile
 	pauseImage := images.Pause(kv, imageRepository)
 
-	c := exec.Command("/bin/bash", "-c", fmt.Sprintf("sudo sed -e 's|^pause_image = .*$|pause_image = \"%s\"|' -i %s", pauseImage, cPath))
+	c := exec.Command("/bin/bash", "-c", fmt.Sprintf("sudo sed -e 's|^pause_image = .*$|pause_image = \"%s\"|' -i %s", pauseImage, crioConfigFile))
 	if _, err := cr.RunCmd(c); err != nil {
 		return errors.Wrap(err, "generateCRIOConfig.")
 	}
@@ -72,6 +71,16 @@ func generateCRIOConfig(cr CommandRunner, imageRepository string, kv semver.Vers
 	return nil
 }
 
+func (r *CRIO) forceSystemd() error {
+	// remove `cgroup_manager` since cri-o defaults to `systemd` if nothing set
+	c := exec.Command("/bin/bash", "-c", fmt.Sprintf("sudo sed -e 's|^cgroup_manager = .*$||' -i %s", crioConfigFile))
+	if _, err := r.Runner.RunCmd(c); err != nil {
+		return errors.Wrap(err, "force systemd")
+	}
+
+	return nil
+}
+
 // Name is a human readable name for CRIO
 func (r *CRIO) Name() string {
 	return "CRI-O"
@@ -139,7 +148,7 @@ func enableIPForwarding(cr CommandRunner) error {
 }
 
 // Enable idempotently enables CRIO on a host
-func (r *CRIO) Enable(disOthers, _, inUserNamespace bool) error {
+func (r *CRIO) Enable(disOthers, forceSystemd, inUserNamespace bool) error {
 	if inUserNamespace {
 		return errors.New("inUserNamespace must not be true for cri-o (yet)")
 	}
@@ -157,6 +166,11 @@ func (r *CRIO) Enable(disOthers, _, inUserNamespace bool) error {
 	if err := enableIPForwarding(r.Runner); err != nil {
 		return err
 	}
+	if forceSystemd {
+		if err := r.forceSystemd(); err != nil {
+			return err
+		}
+	}
 	return r.Init.Start("crio")
 }
 
diff --git a/test/integration/docker_test.go b/test/integration/docker_test.go
index db1f43862138..4b7667690267 100644
--- a/test/integration/docker_test.go
+++ b/test/integration/docker_test.go
@@ -94,6 +94,8 @@ func TestForceSystemdFlag(t *testing.T) {
 		validateDockerSystemd(ctx, t, profile)
 	case "containerd":
 		validateContainerdSystemd(ctx, t, profile)
+	case "crio":
+		validateCrioSystemd(ctx, t, profile)
 	}
 
 }
@@ -113,13 +115,25 @@ func validateDockerSystemd(ctx context.Context, t *testing.T, profile string) {
 func validateContainerdSystemd(ctx context.Context, t *testing.T, profile string) {
 	rr, err := Run(t, exec.CommandContext(ctx, Target(), "-p", profile, "ssh", "cat /etc/containerd/config.toml"))
 	if err != nil {
-		t.Errorf("failed to get docker cgroup driver. args %q: %v", rr.Command(), err)
+		t.Errorf("failed to get containerd cgroup driver. args %q: %v", rr.Command(), err)
 	}
 	if !strings.Contains(rr.Output(), "SystemdCgroup = true") {
 		t.Fatalf("expected systemd cgroup driver, got: %v", rr.Output())
 	}
 }
 
+// validateCrioSystemd makes sure the --force-systemd flag worked with the cri-o container runtime
+func validateCrioSystemd(ctx context.Context, t *testing.T, profile string) {
+	rr, err := Run(t, exec.CommandContext(ctx, Target(), "-p", profile, "ssh", "cat /etc/crio/crio.conf"))
+	if err != nil {
+		t.Errorf("failed to get cri-o cgroup driver. args %q: %v", rr.Command(), err)
+	}
+	// cri-o defaults to `systemd` if `cgroup_manager` not set, so we remove `cgroup_manager` on force
+	if strings.Contains(rr.Output(), "cgroup_manager = ") {
+		t.Fatalf("expected systemd cgroup driver, got: %v", rr.Output())
+	}
+}
+
 // TestForceSystemdEnv makes sure the MINIKUBE_FORCE_SYSTEMD environment variable works just as well as the --force-systemd flag
 func TestForceSystemdEnv(t *testing.T) {
 	if NoneDriver() {