diff --git a/pkg/runtime/core/trainingruntime.go b/pkg/runtime/core/trainingruntime.go
index 807d9847e6..185ac5fd69 100644
--- a/pkg/runtime/core/trainingruntime.go
+++ b/pkg/runtime/core/trainingruntime.go
@@ -166,13 +166,17 @@ func (r *TrainingRuntime) newRuntimeInfo(
 	}
 
 	for i, rJob := range jobSetSpecApply.ReplicatedJobs {
-		// TODO: Support multiple replicas ('.template.spec.replicatedJobs[*].replicas') for replicated Jobs.
+		// TODO: Support multiple replicas for non-trainer replicatedJobs.
 		// REF: https://github.com/kubeflow/trainer/issues/2318
 		count := ptr.Deref(rJob.Template.Spec.Parallelism, 1)
 		var ancestor *string
 		if metadata := rJob.Template.ObjectMetaApplyConfiguration; metadata != nil && metadata.Labels != nil {
 			if labelAncestor, ok := metadata.Labels[constants.LabelTrainJobAncestor]; ok {
 				if labelAncestor == constants.AncestorTrainer && mlPolicy != nil {
+					// For multi-slice TPU, numNodes represents total nodes across all slices.
+					// Per-slice Parallelism/Completions is computed in Build() by dividing
+					// the final count (set by EnforceMLPolicy) by trainer replicas.
+					// REF: https://github.com/kubeflow/trainer/issues/3407
 					count = ptr.Deref(mlPolicy.NumNodes, 1)
 
 					// Apply resourcesPerNode from TrainJob to the template spec
diff --git a/pkg/runtime/core/trainingruntime_test.go b/pkg/runtime/core/trainingruntime_test.go
index e933ec844f..0e2c8b1756 100644
--- a/pkg/runtime/core/trainingruntime_test.go
+++ b/pkg/runtime/core/trainingruntime_test.go
@@ -116,6 +116,56 @@ func TestTrainingRuntimeNewObjects(t *testing.T) {
 					Obj(),
 			},
 		},
+		"succeeded to build PodGroup and JobSet with multi-slice TPU trainer.": {
+			trainingRuntime: testingutil.MakeTrainingRuntimeWrapper(metav1.NamespaceDefault, "test-runtime").
+				RuntimeSpec(
+					testingutil.MakeTrainingRuntimeSpecWrapper(testingutil.MakeTrainingRuntimeWrapper(metav1.NamespaceDefault, "test-runtime").Spec).
+						WithMLPolicy(
+							testingutil.MakeMLPolicyWrapper().
+								WithNumNodes(32).
+								Obj(),
+						).
+						PodGroupPolicyCoschedulingSchedulingTimeout(120).
+						Replicas(4, constants.Node).
+						Container(constants.DatasetInitializer, constants.DatasetInitializer, "test:runtime", []string{"runtime"}, []string{"runtime"}, resRequests).
+						Container(constants.ModelInitializer, constants.ModelInitializer, "test:runtime", []string{"runtime"}, []string{"runtime"}, resRequests).
+						Container(constants.Node, constants.Node, "test:runtime", []string{"runtime"}, []string{"runtime"}, resRequests).
+						Obj(),
+				).Obj(),
+			trainJob: testingutil.MakeTrainJobWrapper(metav1.NamespaceDefault, "test-job").
+				UID("uid").
+				RuntimeRef(trainer.SchemeGroupVersion.WithKind(trainer.TrainingRuntimeKind), "test-runtime").
+				Trainer(
+					testingutil.MakeTrainJobTrainerWrapper().
+						NumNodes(32).
+						Obj(),
+				).
+				Obj(),
+			wantObjs: []runtime.Object{
+				testingutil.MakeJobSetWrapper(metav1.NamespaceDefault, "test-job").
+					ControllerReference(trainer.SchemeGroupVersion.WithKind(trainer.TrainJobKind), "test-job", "uid").
+					Replicas(4, constants.Node).
+					Replicas(1, constants.DatasetInitializer, constants.ModelInitializer, constants.Launcher).
+					Parallelism(8, constants.Node).
+					Parallelism(1, constants.DatasetInitializer, constants.ModelInitializer, constants.Launcher).
+					Completions(8, constants.Node).
+					Completions(1, constants.DatasetInitializer, constants.ModelInitializer, constants.Launcher).
+					NumNodes(8).
+					Container(constants.DatasetInitializer, constants.DatasetInitializer, "test:runtime", []string{"runtime"}, []string{"runtime"}, resRequests).
+					Container(constants.ModelInitializer, constants.ModelInitializer, "test:runtime", []string{"runtime"}, []string{"runtime"}, resRequests).
+					Container(constants.Node, constants.Node, "test:runtime", []string{"runtime"}, []string{"runtime"}, resRequests).
+					PodLabel(schedulerpluginsv1alpha1.PodGroupLabel, "test-job").
+					Obj(),
+				testingutil.MakeSchedulerPluginsPodGroup(metav1.NamespaceDefault, "test-job").
+					ControllerReference(trainer.SchemeGroupVersion.WithKind(trainer.TrainJobKind), "test-job", "uid").
+					MinMember(34). // 34 = 8 nodes × 4 slices + 1 DatasetInitializer + 1 ModelInitializer
+					MinResources(corev1.ResourceList{
+						corev1.ResourceCPU: resource.MustParse("34"),
+					}).
+					SchedulingTimeout(120).
+					Obj(),
+			},
+		},
 		"succeeded to build JobSet with NumNodes from the Runtime and container from the TrainJob.": {
 			trainingRuntime: testingutil.MakeTrainingRuntimeWrapper(metav1.NamespaceDefault, "test-runtime").RuntimeSpec(
 				testingutil.MakeTrainingRuntimeSpecWrapper(testingutil.MakeTrainingRuntimeWrapper(metav1.NamespaceDefault, "test-runtime").Spec).
diff --git a/pkg/runtime/framework/plugins/jobset/builder.go b/pkg/runtime/framework/plugins/jobset/builder.go
index d5d8e1ca86..999848b1a8 100644
--- a/pkg/runtime/framework/plugins/jobset/builder.go
+++ b/pkg/runtime/framework/plugins/jobset/builder.go
@@ -118,9 +118,11 @@ func (b *Builder) Trainer(info *runtime.Info, trainJob *trainer.TrainJob) *Build
 			ancestor = jobMetadata.Labels[constants.LabelTrainJobAncestor]
 		}
 		if ancestor == constants.AncestorTrainer {
-			// TODO: Support multiple replicas ('.template.spec.replicatedJobs[*].replicas') for replicated Jobs.
-			// REF: https://github.com/kubeflow/trainer/issues/2318
-			b.Spec.ReplicatedJobs[i].Replicas = ptr.To[int32](1)
+			// Preserve replicas for multi-slice TPU support.
+			// REF: https://github.com/kubeflow/trainer/issues/3407
+			if b.Spec.ReplicatedJobs[i].Replicas == nil {
+				b.Spec.ReplicatedJobs[i].Replicas = ptr.To[int32](1)
+			}
 			// Update values for the Trainer container.
 			for j, container := range rJob.Template.Spec.Template.Spec.Containers {
 				if *container.Name == constants.Node {
diff --git a/pkg/runtime/framework/plugins/jobset/jobset.go b/pkg/runtime/framework/plugins/jobset/jobset.go
index a629c6fcc8..ceafd9b80c 100644
--- a/pkg/runtime/framework/plugins/jobset/jobset.go
+++ b/pkg/runtime/framework/plugins/jobset/jobset.go
@@ -273,8 +273,27 @@ func (j *JobSet) Build(ctx context.Context, info *runtime.Info, trainJob *traine
 
 	for psIdx, ps := range info.TemplateSpec.PodSets {
 		if ps.Count != nil {
-			jobSetSpec.ReplicatedJobs[psIdx].Template.Spec.Parallelism = ps.Count
-			jobSetSpec.ReplicatedJobs[psIdx].Template.Spec.Completions = ps.Count
+			rJob := &jobSetSpec.ReplicatedJobs[psIdx]
+			jobMetadata := rJob.Template.ObjectMetaApplyConfiguration
+			isTrainer := jobMetadata != nil && jobMetadata.Labels != nil &&
+				jobMetadata.Labels[constants.LabelTrainJobAncestor] == constants.AncestorTrainer
+			if isTrainer {
+				// For multi-slice trainer: count = numNodes (total across all slices).
+				// Parallelism/Completions must be per-slice = numNodes / replicas.
+				replicas := ptr.Deref(rJob.Replicas, 1)
+				if replicas <= 0 {
+					return nil, fmt.Errorf("trainer replicatedJob %d has invalid replicas %d: must be > 0", psIdx, replicas)
+				}
+				if *ps.Count%replicas != 0 {
+					return nil, fmt.Errorf("trainer numNodes %d must be evenly divisible by replicas %d", *ps.Count, replicas)
+				}
+				perSlice := *ps.Count / replicas
+				rJob.Template.Spec.Parallelism = &perSlice
+				rJob.Template.Spec.Completions = &perSlice
+			} else {
+				rJob.Template.Spec.Parallelism = ps.Count
+				rJob.Template.Spec.Completions = ps.Count
+			}
 		}
 		apply.UpsertVolumes(&jobSetSpec.ReplicatedJobs[psIdx].Template.Spec.Template.Spec.Volumes, ps.Volumes...)
 		for containerIdx, container := range ps.Containers {
diff --git a/pkg/webhooks/trainingruntime_webhook.go b/pkg/webhooks/trainingruntime_webhook.go
index 14f1fc3594..9b6f14160c 100644
--- a/pkg/webhooks/trainingruntime_webhook.go
+++ b/pkg/webhooks/trainingruntime_webhook.go
@@ -76,7 +76,7 @@ func validateReplicatedJobs(rJobs []jobsetv1alpha2.ReplicatedJob) field.ErrorLis
 		}
 
 		if labelAncestor, ok := rJob.Template.Labels[constants.LabelTrainJobAncestor]; ok && ancestors.Has(labelAncestor) {
-			if rJob.Replicas != 1 {
+			if labelAncestor != constants.AncestorTrainer && rJob.Replicas != 1 {
 				allErrs = append(allErrs, field.Invalid(rJobsPath.Index(idx).Child("replicas"), rJob.Replicas, rJobReplicasErrorMsg))
 			}
 
diff --git a/pkg/webhooks/trainingruntime_webhook_test.go b/pkg/webhooks/trainingruntime_webhook_test.go
index fb39f0600d..ca0b00d963 100644
--- a/pkg/webhooks/trainingruntime_webhook_test.go
+++ b/pkg/webhooks/trainingruntime_webhook_test.go
@@ -56,8 +56,6 @@ func TestValidateReplicatedJobs(t *testing.T) {
 					"2", ""),
 				field.Invalid(field.NewPath("spec").Child("template").Child("spec").Child("replicatedJobs").Index(1).Child("replicas"),
 					"2", ""),
-				field.Invalid(field.NewPath("spec").Child("template").Child("spec").Child("replicatedJobs").Index(3).Child("replicas"),
-					"2", ""),
 			},
 		},
 		"missing required container in replicatedJobs": {