diff --git a/beacon-chain/state/stategen/migrate.go b/beacon-chain/state/stategen/migrate.go
index e8985e5e76e4..be4f5fbd28f8 100644
--- a/beacon-chain/state/stategen/migrate.go
+++ b/beacon-chain/state/stategen/migrate.go
@@ -4,10 +4,12 @@ import (
 	"context"
 	"encoding/hex"
 	"fmt"
+	"slices"
 
 	"github.com/OffchainLabs/prysm/v7/beacon-chain/core/transition"
 	"github.com/OffchainLabs/prysm/v7/beacon-chain/state"
 	"github.com/OffchainLabs/prysm/v7/config/features"
+	"github.com/OffchainLabs/prysm/v7/consensus-types/interfaces"
 	"github.com/OffchainLabs/prysm/v7/consensus-types/primitives"
 	"github.com/OffchainLabs/prysm/v7/encoding/bytesutil"
 	"github.com/OffchainLabs/prysm/v7/monitoring/tracing/trace"
@@ -128,11 +130,19 @@ func (s *State) MigrateToCold(ctx context.Context, fRoot [32]byte) error {
 func (s *State) migrateToColdHdiff(ctx context.Context, fRoot [32]byte) error {
 	s.finalizedInfo.lock.RLock()
 	oldFSlot := s.finalizedInfo.slot
+	oldFRoot := s.finalizedInfo.root
+	oldFState := s.finalizedInfo.state
 	s.finalizedInfo.lock.RUnlock()
 	fSlot, err := s.beaconDB.SlotByBlockRoot(ctx, fRoot)
 	if err != nil {
 		return errors.Wrap(err, "could not get slot by block root")
 	}
+
+	if oldFState == nil || oldFState.IsNil() {
+		return errors.New("finalized state is nil")
+	}
+
+	slotsToSave := make([]primitives.Slot, 0)
 	for slot := oldFSlot; slot < fSlot; slot++ {
 		if ctx.Err() != nil {
 			return ctx.Err()
@@ -148,58 +158,82 @@ func (s *State) migrateToColdHdiff(ctx context.Context, fRoot [32]byte) error {
 		if uint64(slot) == offset {
 			continue
 		}
-		// The state needs to be saved.
-		// Try the epoch boundary cache first.
-		cached, exists, err := s.epochBoundaryStateCache.getBySlot(slot)
+		slotsToSave = append(slotsToSave, slot)
+	}
+
+	if len(slotsToSave) == 0 {
+		// Update finalized info in memory.
+		fInfo, ok, err := s.epochBoundaryStateCache.getByBlockRoot(fRoot)
 		if err != nil {
-			log.WithError(err).Errorf("could not get epoch boundary state for slot %d", slot)
-			cached = nil
-			exists = false
+			return err
 		}
-		var aRoot [32]byte
-		var aState state.BeaconState
-		if exists {
-			aRoot = cached.root
-			aState = cached.state
-		} else {
-			_, roots, err := s.beaconDB.HighestRootsBelowSlot(ctx, slot)
+		if ok {
+			s.SaveFinalizedState(fSlot, fRoot, fInfo.state)
+		}
+		return nil
+	}
+
+	blocks, err := s.loadBlocks(ctx, oldFSlot+1, fSlot, fRoot)
+	if err != nil {
+		return errors.Wrap(err, "could not load blocks for hdiff migration")
+	}
+	slices.SortFunc(blocks, func(a, b interfaces.ReadOnlySignedBeaconBlock) int {
+		switch {
+		case a.Block().Slot() < b.Block().Slot():
+			return -1
+		case a.Block().Slot() > b.Block().Slot():
+			return 1
+		default:
+			return 0
+		}
+	})
+
+	currState := oldFState.Copy()
+	currRoot := oldFRoot
+	nextBlockIdx := 0
+
+	for _, slot := range slotsToSave {
+		if ctx.Err() != nil {
+			return ctx.Err()
+		}
+
+		// Replay all canonical blocks up to target slot.
+		for nextBlockIdx < len(blocks) && blocks[nextBlockIdx].Block().Slot() <= slot {
+			currState, err = executeStateTransitionStateGen(ctx, currState, blocks[nextBlockIdx])
 			if err != nil {
-				return err
+				return errors.Wrapf(err, "could not replay block at slot %d during hdiff migration", blocks[nextBlockIdx].Block().Slot())
 			}
-			// Given the block has been finalized, the db should not have more than one block in a given slot.
-			// We should error out when this happens.
-			if len(roots) != 1 {
-				return errUnknownBlock
-			}
-			aRoot = roots[0]
-			// Different than the legacy MigrateToCold, we need to always get the state even if
-			// the state exists in DB as part of the hot state db, because we need to process slots
-			// to the state diff tree slots.
-			aState, err = s.StateByRoot(ctx, aRoot)
+			currRoot, err = blocks[nextBlockIdx].Block().HashTreeRoot()
 			if err != nil {
-				return err
+				return errors.Wrap(err, "could not compute block root during hdiff migration")
 			}
+			nextBlockIdx++
 		}
-		if s.beaconDB.HasState(ctx, aRoot) {
-			s.migrateHotToCold(aRoot)
-			continue
-		}
-		// advance slots to the target slot
-		if aState.Slot() < slot {
-			aState, err = transition.ProcessSlots(ctx, aState, slot)
+
+		// If target slot is skipped, advance with process slots.
+		if currState.Slot() < slot {
+			currState, err = transition.ProcessSlots(ctx, currState, slot)
 			if err != nil {
-				return errors.Wrapf(err, "could not process slots to slot %d", slot)
+				return errors.Wrapf(err, "could not process slots to slot %d during hdiff migration", slot)
 			}
 		}
-		if err := s.beaconDB.SaveState(ctx, aState, aRoot); err != nil {
+		if currState.Slot() != slot {
+			return errors.Errorf("unexpected replay state slot %d while targeting %d", currState.Slot(), slot)
+		}
+
+		// Save to the finalized state-diff tree. This does not store unfinalized states in the diff tree
+		// because migration only runs after finalized checkpoint advancement.
+		if err := s.beaconDB.SaveState(ctx, currState, currRoot); err != nil {
 			return err
 		}
+		s.migrateHotToCold(currRoot)
 		log.WithFields(
 			logrus.Fields{
-				"slot": aState.Slot(),
-				"root": fmt.Sprintf("%#x", aRoot),
+				"slot": currState.Slot(),
+				"root": fmt.Sprintf("%#x", currRoot),
 			}).Info("Saved state in DB")
 	}
+
 	// Update finalized info in memory.
 	fInfo, ok, err := s.epochBoundaryStateCache.getByBlockRoot(fRoot)
 	if err != nil {