diff --git a/api/v1alpha1/stage_types.go b/api/v1alpha1/stage_types.go
index 9f5343519b..d2912f045f 100644
--- a/api/v1alpha1/stage_types.go
+++ b/api/v1alpha1/stage_types.go
@@ -154,8 +154,12 @@ type Stage struct {
 // orchestrates the promotion of Freight from one or more upstream Stages to
 // one or more downstream Stages.
 func (s *Stage) IsControlFlow() bool {
+	if s == nil {
+		return false
+	}
+
 	switch {
-	case s.Spec.PromotionTemplateRef != nil && len(s.Spec.PromotionTemplate.Name) > 0:
+	case s.Spec.PromotionTemplateRef != nil && len(s.Spec.PromotionTemplateRef.Name) > 0:
 		return false
 	case s.Spec.PromotionTemplate != nil && len(s.Spec.PromotionTemplate.Spec.Steps) > 0:
 		return false
diff --git a/internal/api/promote_downstream_v1alpha1.go b/internal/api/promote_downstream_v1alpha1.go
index 7b745df629..cedc05f27b 100644
--- a/internal/api/promote_downstream_v1alpha1.go
+++ b/internal/api/promote_downstream_v1alpha1.go
@@ -154,7 +154,7 @@ func (s *server) PromoteDownstream(
 			var ok bool
 			if template, ok = templates[downstream.Spec.PromotionTemplateRef.Name]; !ok {
 				template = &kargoapi.PromotionTemplate{}
-				if err = s.client.Get(ctx, types.NamespacedName{
+				if err = s.getPromotionTemplateFn(ctx, types.NamespacedName{
 					Namespace: downstream.Namespace,
 					Name:      downstream.Spec.PromotionTemplateRef.Name,
 				}, template); err != nil {
diff --git a/internal/api/promote_downstream_v1alpha1_test.go b/internal/api/promote_downstream_v1alpha1_test.go
index 1c30b91fc2..893ce68f11 100644
--- a/internal/api/promote_downstream_v1alpha1_test.go
+++ b/internal/api/promote_downstream_v1alpha1_test.go
@@ -442,6 +442,93 @@ func TestPromoteDownstream(t *testing.T) {
 				require.Equal(t, "not authorized", err.Error())
 			},
 		},
+		{
+			name: "PromotionTemplate reference not found",
+			req: &svcv1alpha1.PromoteDownstreamRequest{
+				Project: "fake-project",
+				Stage:   "fake-stage",
+				Freight: "fake-freight",
+			},
+			server: &server{
+				validateProjectExistsFn: func(context.Context, string) error {
+					return nil
+				},
+				getStageFn: func(
+					context.Context,
+					client.Client,
+					types.NamespacedName,
+				) (*kargoapi.Stage, error) {
+					return &kargoapi.Stage{
+						ObjectMeta: metav1.ObjectMeta{
+							Namespace: "fake-project",
+							Name:      "fake-stage",
+						},
+						Spec: testStageSpec,
+					}, nil
+				},
+				getFreightByNameOrAliasFn: func(
+					context.Context,
+					client.Client,
+					string, string, string,
+				) (*kargoapi.Freight, error) {
+					return &kargoapi.Freight{
+						Status: kargoapi.FreightStatus{
+							VerifiedIn: map[string]kargoapi.VerifiedStage{
+								"fake-stage": {},
+							},
+						},
+					}, nil
+				},
+				getPromotionTemplateFn: func(
+					context.Context,
+					client.ObjectKey,
+					client.Object,
+					...client.GetOption,
+				) error {
+					return errors.New("not found")
+				},
+				findDownstreamStagesFn: func(
+					context.Context,
+					*kargoapi.Stage,
+					kargoapi.FreightOrigin,
+				) ([]kargoapi.Stage, error) {
+					return []kargoapi.Stage{
+						{
+							Spec: kargoapi.StageSpec{
+								PromotionTemplateRef: &kargoapi.PromotionTemplateReference{
+									Name: "fake-promotion-template",
+								},
+							},
+						},
+					}, nil
+				},
+				authorizeFn: func(
+					context.Context,
+					string,
+					schema.GroupVersionResource,
+					string,
+					client.ObjectKey,
+				) error {
+					return nil
+				},
+				createPromotionFn: func(
+					context.Context,
+					client.Object,
+					...client.CreateOption,
+				) error {
+					return nil
+				},
+			},
+			assertions: func(
+				t *testing.T,
+				_ *fakeevent.EventRecorder,
+				_ *connect.Response[svcv1alpha1.PromoteDownstreamResponse],
+				err error,
+			) {
+				require.ErrorContains(t, err, "get PromotionTemplate")
+				require.ErrorContains(t, err, "not found")
+			},
+		},
 		{
 			name: "error creating Promotion",
 			req: &svcv1alpha1.PromoteDownstreamRequest{
diff --git a/internal/api/promote_to_stage_v1alpha1.go b/internal/api/promote_to_stage_v1alpha1.go
index 6522309b39..341f763e6e 100644
--- a/internal/api/promote_to_stage_v1alpha1.go
+++ b/internal/api/promote_to_stage_v1alpha1.go
@@ -125,7 +125,7 @@ func (s *server) PromoteToStage(
 		}
 
 		template = &kargoapi.PromotionTemplate{}
-		if err = s.client.Get(ctx, types.NamespacedName{
+		if err = s.getPromotionTemplateFn(ctx, types.NamespacedName{
 			Namespace: project,
 			Name:      stage.Spec.PromotionTemplateRef.Name,
 		}, template); err != nil {
diff --git a/internal/api/promote_to_stage_v1alpha1_test.go b/internal/api/promote_to_stage_v1alpha1_test.go
index c25b50c194..81bc507dfc 100644
--- a/internal/api/promote_to_stage_v1alpha1_test.go
+++ b/internal/api/promote_to_stage_v1alpha1_test.go
@@ -81,8 +81,7 @@ func TestPromoteToStage(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteToStageResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "something went wrong", err.Error())
+				require.ErrorContains(t, err, "something went wrong")
 			},
 		},
 		{
@@ -110,8 +109,7 @@ func TestPromoteToStage(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteToStageResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "get stage: something went wrong", err.Error())
+				require.ErrorContains(t, err, "get stage: something went wrong")
 			},
 		},
 		{
@@ -181,8 +179,7 @@ func TestPromoteToStage(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteToStageResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "get freight: something went wrong", err.Error())
+				require.ErrorContains(t, err, "get freight: something went wrong")
 			},
 		},
 		{
@@ -320,8 +317,77 @@ func TestPromoteToStage(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteToStageResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "not authorized", err.Error())
+				require.ErrorContains(t, err, "not authorized")
+			},
+		},
+		{
+			name: "PromotionTemplate not found",
+			req: &svcv1alpha1.PromoteToStageRequest{
+				Project: "fake-project",
+				Stage:   "fake-stage",
+				Freight: "fake-freight",
+			},
+			server: &server{
+				validateProjectExistsFn: func(context.Context, string) error {
+					return nil
+				},
+				getStageFn: func(
+					context.Context,
+					client.Client,
+					types.NamespacedName,
+				) (*kargoapi.Stage, error) {
+					return &kargoapi.Stage{
+						Spec: kargoapi.StageSpec{
+							PromotionTemplateRef: &kargoapi.PromotionTemplateReference{
+								Name: "fake-promotion-template",
+							},
+							RequestedFreight: testStageSpec.RequestedFreight,
+						},
+					}, nil
+				},
+				getPromotionTemplateFn: func(
+					context.Context,
+					client.ObjectKey,
+					client.Object,
+					...client.GetOption,
+				) error {
+					return errors.New("not found")
+				},
+				getFreightByNameOrAliasFn: func(
+					context.Context,
+					client.Client,
+					string, string, string,
+				) (*kargoapi.Freight, error) {
+					return &kargoapi.Freight{}, nil
+				},
+				isFreightAvailableFn: func(*kargoapi.Stage, *kargoapi.Freight) bool {
+					return true
+				},
+				authorizeFn: func(
+					context.Context,
+					string,
+					schema.GroupVersionResource,
+					string,
+					client.ObjectKey,
+				) error {
+					return nil
+				},
+				createPromotionFn: func(
+					context.Context,
+					client.Object,
+					...client.CreateOption,
+				) error {
+					return nil
+				},
+			},
+			assertions: func(
+				t *testing.T,
+				_ *fakeevent.EventRecorder,
+				_ *connect.Response[svcv1alpha1.PromoteToStageResponse],
+				err error,
+			) {
+				require.ErrorContains(t, err, "get PromotionTemplate")
+				require.ErrorContains(t, err, "not found")
 			},
 		},
 		{
@@ -377,8 +443,7 @@ func TestPromoteToStage(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteToStageResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "create promotion: something went wrong", err.Error())
+				require.ErrorContains(t, err, "create promotion: something went wrong")
 			},
 		},
 		{
diff --git a/internal/api/server.go b/internal/api/server.go
index 0a53283f23..3d9a1d5bfa 100644
--- a/internal/api/server.go
+++ b/internal/api/server.go
@@ -69,6 +69,12 @@ type server struct {
 		client.Client,
 		types.NamespacedName,
 	) (*kargoapi.Stage, error)
+	getPromotionTemplateFn func(
+		context.Context,
+		client.ObjectKey,
+		client.Object,
+		...client.GetOption,
+	) error
 	getFreightByNameOrAliasFn func(
 		ctx context.Context,
 		c client.Client,
@@ -175,6 +181,7 @@ func NewServer(
 	s.getFreightByNameOrAliasFn = kargoapi.GetFreightByNameOrAlias
 	s.isFreightAvailableFn = kargoapi.IsFreightAvailable
 	s.createPromotionFn = kubeClient.Create
+	s.getPromotionTemplateFn = kubeClient.Get
 	s.findDownstreamStagesFn = s.findDownstreamStages
 	s.listFreightFn = kubeClient.List
 	s.getAvailableFreightForStageFn = s.getAvailableFreightForStage