diff --git a/internal/backend/runtime/omni/validated/state.go b/internal/backend/runtime/omni/validated/state.go
index e3c9762cb..7a154b20a 100644
--- a/internal/backend/runtime/omni/validated/state.go
+++ b/internal/backend/runtime/omni/validated/state.go
@@ -105,17 +105,32 @@ func (v *State) Update(ctx context.Context, newResource resource.Resource, opts
 		return err
 	}
 
+	var validationErrs error
+
 	// if the existing resource was not found, instead of returning the not found error, run the validations first
 	// only if the validations pass, return the not found error
 
-	var validationErrs error
-
 	for _, validation := range v.updateValidations {
 		if validationErr := validation(ctx, existing, newResource, opts...); validationErr != nil {
 			validationErrs = multierror.Append(validationErrs, validationErr)
 		}
 	}
 
+	// If the resource is tearing down, run the destroy validations as well
+	if newResource.Metadata().Phase() == resource.PhaseTearingDown {
+		updateOpts := state.UpdateOptions{}
+
+		for _, opt := range opts {
+			opt(&updateOpts)
+		}
+
+		for _, validation := range v.destroyValidations {
+			if validationErr := validation(ctx, newResource.Metadata(), existing, state.WithDestroyOwner(updateOpts.Owner)); validationErr != nil {
+				validationErrs = multierror.Append(validationErrs, validationErr)
+			}
+		}
+	}
+
 	if validationErrs != nil {
 		return ValidationError(validationErrs)
 	}
diff --git a/internal/backend/runtime/omni/validated/state_test.go b/internal/backend/runtime/omni/validated/state_test.go
index 3c54a5556..cbbba0a40 100644
--- a/internal/backend/runtime/omni/validated/state_test.go
+++ b/internal/backend/runtime/omni/validated/state_test.go
@@ -13,11 +13,13 @@ import (
 	"time"
 
 	"github.com/cosi-project/runtime/pkg/resource"
+	"github.com/cosi-project/runtime/pkg/safe"
 	"github.com/cosi-project/runtime/pkg/state"
 	"github.com/cosi-project/runtime/pkg/state/impl/inmem"
 	"github.com/cosi-project/runtime/pkg/state/impl/namespaced"
 	"github.com/hashicorp/go-multierror"
 	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
 
 	"github.com/siderolabs/omni/client/pkg/omni/resources"
 	"github.com/siderolabs/omni/client/pkg/omni/resources/omni"
@@ -205,3 +207,41 @@ func TestValidations(t *testing.T) {
 	_, err = innerSt.Get(ctx, machine.Metadata())
 	assert.True(t, state.IsNotFoundError(err))
 }
+
+func TestTeardownDestroyValidations(t *testing.T) {
+	innerSt := state.WrapCore(namespaced.NewState(inmem.Build))
+	st := state.WrapCore(
+		validated.NewState(innerSt,
+			validated.WithUpdateValidations(func(context.Context, resource.Resource, resource.Resource, ...state.UpdateOption) error {
+				return errors.New("update")
+			}), validated.WithDestroyValidations(func(_ context.Context, _ resource.Pointer, _ resource.Resource, option ...state.DestroyOption) error {
+				opts := state.DestroyOptions{}
+
+				for _, opt := range option {
+					opt(&opts)
+				}
+
+				return errors.New("destroy by " + opts.Owner)
+			}),
+		),
+	)
+
+	res := omni.NewCluster(resources.DefaultNamespace, "something")
+
+	require.NoError(t, st.Create(context.Background(), res))
+
+	ctx, cancel := context.WithTimeout(context.Background(), 3*time.Second)
+	t.Cleanup(cancel)
+
+	_, err := safe.StateUpdateWithConflicts(ctx, st, res.Metadata(), func(res *omni.Cluster) error {
+		res.TypedSpec().Value.TalosVersion = "1234"
+
+		return nil
+	})
+	require.EqualError(t, err, "failed to validate: 1 error occurred:\n\t* update\n\n")
+
+	const teardownOwner = "foobar-controller"
+
+	_, err = st.Teardown(ctx, res.Metadata(), state.WithTeardownOwner(teardownOwner))
+	require.EqualError(t, err, fmt.Sprintf("failed to validate: 2 errors occurred:\n\t* update\n\t* destroy by %s\n\n", teardownOwner))
+}