diff --git a/internal/api/promote_downstream_v1alpha1_test.go b/internal/api/promote_downstream_v1alpha1_test.go
index 1c30b91fc2..af37308696 100644
--- a/internal/api/promote_downstream_v1alpha1_test.go
+++ b/internal/api/promote_downstream_v1alpha1_test.go
@@ -30,6 +30,7 @@ func TestPromoteDownstream(t *testing.T) {
 			},
 		}},
 	}
+
 	testCases := []struct {
 		name       string
 		req        *svcv1alpha1.PromoteDownstreamRequest
@@ -74,8 +75,7 @@ func TestPromoteDownstream(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteDownstreamResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "something went wrong", err.Error())
+				require.ErrorContains(t, err, "something went wrong")
 			},
 		},
 		{
@@ -103,8 +103,7 @@ func TestPromoteDownstream(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteDownstreamResponse],
 				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")
 			},
 		},
 		{
@@ -174,8 +173,7 @@ func TestPromoteDownstream(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteDownstreamResponse],
 				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")
 			},
 		},
 		{
@@ -313,8 +311,7 @@ func TestPromoteDownstream(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteDownstreamResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "find downstream stages: something went wrong", err.Error())
+				require.ErrorContains(t, err, "find downstream stages: something went wrong")
 			},
 		},
 		{
@@ -438,8 +435,87 @@ func TestPromoteDownstream(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteDownstreamResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "not authorized", err.Error())
+				require.ErrorContains(t, err, "not authorized")
+			},
+		},
+		{
+			name: "error building Promotion",
+			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
+				},
+				findDownstreamStagesFn: func(
+					context.Context,
+					*kargoapi.Stage,
+					kargoapi.FreightOrigin,
+				) ([]kargoapi.Stage, error) {
+					return []kargoapi.Stage{
+						{
+							Spec: kargoapi.StageSpec{
+								PromotionTemplate: &kargoapi.PromotionTemplate{
+									Spec: kargoapi.PromotionTemplateSpec{
+										Steps: []kargoapi.PromotionStep{{}},
+									},
+								},
+							},
+						},
+					}, 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, "stage is required")
 			},
 		},
 		{
@@ -472,6 +548,10 @@ func TestPromoteDownstream(t *testing.T) {
 					string, string, string,
 				) (*kargoapi.Freight, error) {
 					return &kargoapi.Freight{
+						ObjectMeta: metav1.ObjectMeta{
+							Namespace: "fake-project",
+							Name:      "fake-freight",
+						},
 						Status: kargoapi.FreightStatus{
 							VerifiedIn: map[string]kargoapi.VerifiedStage{
 								"fake-stage": {},
@@ -486,6 +566,10 @@ func TestPromoteDownstream(t *testing.T) {
 				) ([]kargoapi.Stage, error) {
 					return []kargoapi.Stage{
 						{
+							ObjectMeta: metav1.ObjectMeta{
+								Namespace: "fake-project",
+								Name:      "fake-downstream-stage",
+							},
 							Spec: kargoapi.StageSpec{
 								PromotionTemplate: &kargoapi.PromotionTemplate{
 									Spec: kargoapi.PromotionTemplateSpec{
@@ -556,6 +640,10 @@ func TestPromoteDownstream(t *testing.T) {
 					string, string, string,
 				) (*kargoapi.Freight, error) {
 					return &kargoapi.Freight{
+						ObjectMeta: metav1.ObjectMeta{
+							Namespace: "fake-project",
+							Name:      "fake-freight",
+						},
 						Status: kargoapi.FreightStatus{
 							VerifiedIn: map[string]kargoapi.VerifiedStage{
 								"fake-stage": {},
@@ -570,6 +658,10 @@ func TestPromoteDownstream(t *testing.T) {
 				) ([]kargoapi.Stage, error) {
 					return []kargoapi.Stage{
 						{
+							ObjectMeta: metav1.ObjectMeta{
+								Namespace: "fake-project",
+								Name:      "fake-downstream-stage",
+							},
 							Spec: kargoapi.StageSpec{
 								PromotionTemplate: &kargoapi.PromotionTemplate{
 									Spec: kargoapi.PromotionTemplateSpec{
diff --git a/internal/api/promote_to_stage_v1alpha1_test.go b/internal/api/promote_to_stage_v1alpha1_test.go
index 99fb960a0f..bd1fdcb78f 100644
--- a/internal/api/promote_to_stage_v1alpha1_test.go
+++ b/internal/api/promote_to_stage_v1alpha1_test.go
@@ -8,6 +8,7 @@ import (
 	"connectrpc.com/connect"
 	"github.com/stretchr/testify/require"
 	corev1 "k8s.io/api/core/v1"
+	metav1 "k8s.io/apimachinery/pkg/apis/meta/v1"
 	"k8s.io/apimachinery/pkg/runtime/schema"
 	"k8s.io/apimachinery/pkg/types"
 	"sigs.k8s.io/controller-runtime/pkg/client"
@@ -28,6 +29,11 @@ func TestPromoteToStage(t *testing.T) {
 				Stages: []string{"fake-upstream-stage"},
 			},
 		}},
+		PromotionTemplate: &kargoapi.PromotionTemplate{
+			Spec: kargoapi.PromotionTemplateSpec{
+				Steps: []kargoapi.PromotionStep{{}},
+			},
+		},
 	}
 	testCases := []struct {
 		name       string
@@ -74,8 +80,7 @@ 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")
 			},
 		},
 		{
@@ -103,8 +108,7 @@ 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")
 			},
 		},
 		{
@@ -174,8 +178,7 @@ 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")
 			},
 		},
 		{
@@ -313,12 +316,11 @@ func TestPromoteToStage(t *testing.T) {
 				_ *connect.Response[svcv1alpha1.PromoteToStageResponse],
 				err error,
 			) {
-				require.Error(t, err)
-				require.Equal(t, "not authorized", err.Error())
+				require.Error(t, err, "not authorized")
 			},
 		},
 		{
-			name: "error creating Promotion",
+			name: "error building Promotion",
 			req: &svcv1alpha1.PromoteToStageRequest{
 				Project: "fake-project",
 				Stage:   "fake-stage",
@@ -334,6 +336,10 @@ func TestPromoteToStage(t *testing.T) {
 					types.NamespacedName,
 				) (*kargoapi.Stage, error) {
 					return &kargoapi.Stage{
+						ObjectMeta: metav1.ObjectMeta{
+							Namespace: "fake-project",
+							Name:      "fake-stage",
+						},
 						Spec: testStageSpec,
 					}, nil
 				},
@@ -356,6 +362,64 @@ func TestPromoteToStage(t *testing.T) {
 				) error {
 					return nil
 				},
+			},
+			assertions: func(
+				t *testing.T,
+				_ *fakeevent.EventRecorder,
+				_ *connect.Response[svcv1alpha1.PromoteToStageResponse],
+				err error,
+			) {
+				require.ErrorContains(t, err, "build promotion")
+			},
+		},
+		{
+			name: "error creating Promotion",
+			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{
+						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{
+						ObjectMeta: metav1.ObjectMeta{
+							Namespace: "fake-project",
+							Name:      "fake-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,
@@ -370,8 +434,7 @@ 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.Error(t, err, "create promotion: something went wrong")
 			},
 		},
 		{
@@ -391,6 +454,10 @@ func TestPromoteToStage(t *testing.T) {
 					types.NamespacedName,
 				) (*kargoapi.Stage, error) {
 					return &kargoapi.Stage{
+						ObjectMeta: metav1.ObjectMeta{
+							Namespace: "fake-project",
+							Name:      "fake-stage",
+						},
 						Spec: testStageSpec,
 					}, nil
 				},
@@ -399,7 +466,12 @@ func TestPromoteToStage(t *testing.T) {
 					client.Client,
 					string, string, string,
 				) (*kargoapi.Freight, error) {
-					return &kargoapi.Freight{}, nil
+					return &kargoapi.Freight{
+						ObjectMeta: metav1.ObjectMeta{
+							Namespace: "fake-project",
+							Name:      "fake-freight",
+						},
+					}, nil
 				},
 				isFreightAvailableFn: func(*kargoapi.Stage, *kargoapi.Freight) bool {
 					return true
diff --git a/internal/controller/stages/regular_stages_test.go b/internal/controller/stages/regular_stages_test.go
index 0d87a194be..ab038a6de0 100644
--- a/internal/controller/stages/regular_stages_test.go
+++ b/internal/controller/stages/regular_stages_test.go
@@ -4342,6 +4342,15 @@ func TestRegularStageReconciler_autoPromoteFreight(t *testing.T) {
 							},
 						},
 					},
+					PromotionTemplate: &kargoapi.PromotionTemplate{
+						Spec: kargoapi.PromotionTemplateSpec{
+							Steps: []kargoapi.PromotionStep{
+								{
+									Uses: "fake-step",
+								},
+							},
+						},
+					},
 				},
 			},
 			objects: []client.Object{
@@ -4555,6 +4564,15 @@ func TestRegularStageReconciler_autoPromoteFreight(t *testing.T) {
 							},
 						},
 					},
+					PromotionTemplate: &kargoapi.PromotionTemplate{
+						Spec: kargoapi.PromotionTemplateSpec{
+							Steps: []kargoapi.PromotionStep{
+								{
+									Uses: "fake-step",
+								},
+							},
+						},
+					},
 				},
 			},
 			objects: []client.Object{
@@ -4616,6 +4634,15 @@ func TestRegularStageReconciler_autoPromoteFreight(t *testing.T) {
 							},
 						},
 					},
+					PromotionTemplate: &kargoapi.PromotionTemplate{
+						Spec: kargoapi.PromotionTemplateSpec{
+							Steps: []kargoapi.PromotionStep{
+								{
+									Uses: "fake-step",
+								},
+							},
+						},
+					},
 				},
 			},
 			objects: []client.Object{
@@ -4693,6 +4720,15 @@ func TestRegularStageReconciler_autoPromoteFreight(t *testing.T) {
 							},
 						},
 					},
+					PromotionTemplate: &kargoapi.PromotionTemplate{
+						Spec: kargoapi.PromotionTemplateSpec{
+							Steps: []kargoapi.PromotionStep{
+								{
+									Uses: "fake-step",
+								},
+							},
+						},
+					},
 				},
 			},
 			objects: []client.Object{
@@ -4777,6 +4813,15 @@ func TestRegularStageReconciler_autoPromoteFreight(t *testing.T) {
 							},
 						},
 					},
+					PromotionTemplate: &kargoapi.PromotionTemplate{
+						Spec: kargoapi.PromotionTemplateSpec{
+							Steps: []kargoapi.PromotionStep{
+								{
+									Uses: "fake-step",
+								},
+							},
+						},
+					},
 				},
 			},
 			objects: []client.Object{
@@ -4842,6 +4887,15 @@ func TestRegularStageReconciler_autoPromoteFreight(t *testing.T) {
 							},
 						},
 					},
+					PromotionTemplate: &kargoapi.PromotionTemplate{
+						Spec: kargoapi.PromotionTemplateSpec{
+							Steps: []kargoapi.PromotionStep{
+								{
+									Uses: "fake-step",
+								},
+							},
+						},
+					},
 				},
 			},
 			objects: []client.Object{
@@ -4890,6 +4944,66 @@ func TestRegularStageReconciler_autoPromoteFreight(t *testing.T) {
 				assert.Len(t, promoList.Items, 1)
 			},
 		},
+		{
+			name: "handles promotion build error",
+			stage: &kargoapi.Stage{
+				ObjectMeta: metav1.ObjectMeta{
+					Namespace: "fake-project",
+					Name:      "test-stage",
+				},
+				Spec: kargoapi.StageSpec{
+					RequestedFreight: []kargoapi.FreightRequest{
+						{
+							Origin: kargoapi.FreightOrigin{
+								Kind: kargoapi.FreightOriginKindWarehouse,
+								Name: "test-warehouse",
+							},
+							Sources: kargoapi.FreightSources{
+								Direct: true,
+							},
+						},
+					},
+					// Missing template to build Promotion
+					PromotionTemplate: nil,
+				},
+			},
+			objects: []client.Object{
+				&kargoapi.Project{
+					ObjectMeta: metav1.ObjectMeta{
+						Name: "fake-project",
+					},
+					Spec: &kargoapi.ProjectSpec{
+						PromotionPolicies: []kargoapi.PromotionPolicy{
+							{
+								Stage:                "test-stage",
+								AutoPromotionEnabled: true,
+							},
+						},
+					},
+				},
+				&kargoapi.Freight{
+					ObjectMeta: metav1.ObjectMeta{
+						Namespace:         "fake-project",
+						Name:              "test-freight",
+						CreationTimestamp: metav1.Time{Time: now},
+					},
+					Origin: kargoapi.FreightOrigin{
+						Kind: kargoapi.FreightOriginKindWarehouse,
+						Name: "test-warehouse",
+					},
+					Status: kargoapi.FreightStatus{},
+				},
+			},
+			assertions: func(
+				t *testing.T,
+				_ *fakeevent.EventRecorder,
+				_ client.Client,
+				_ kargoapi.StageStatus,
+				err error,
+			) {
+				require.ErrorContains(t, err, "error building Promotion")
+			},
+		},
 		{
 			name: "handles promotion creation error",
 			stage: &kargoapi.Stage{
@@ -4909,6 +5023,15 @@ func TestRegularStageReconciler_autoPromoteFreight(t *testing.T) {
 							},
 						},
 					},
+					PromotionTemplate: &kargoapi.PromotionTemplate{
+						Spec: kargoapi.PromotionTemplateSpec{
+							Steps: []kargoapi.PromotionStep{
+								{
+									Uses: "fake-step",
+								},
+							},
+						},
+					},
 				},
 			},
 			objects: []client.Object{