diff --git a/packages/beacon-node/src/api/impl/validator/index.ts b/packages/beacon-node/src/api/impl/validator/index.ts
index ea94cb4b49f7..776034bac020 100644
--- a/packages/beacon-node/src/api/impl/validator/index.ts
+++ b/packages/beacon-node/src/api/impl/validator/index.ts
@@ -1291,12 +1291,20 @@ export function getValidatorApi(
         duties.push({slot: startSlot + i, validatorIndex: indexes[i], pubkey: pubkeys[i]});
       }
 
-      // Returns `null` on the one-off scenario where the genesis block decides its own shuffling.
-      // It should be set to the latest block applied to `self` or the genesis block root.
+      // In v2 the dependent root is different after fulu due to deterministic proposer lookahead.
+      // `head.blockRoot` is used as the dep_root when the decision slot is not yet in
+      // `state.block_roots` (pre-Fulu next-epoch duties from a mid-epoch head state). For the
+      // genesis-decides-its-own-shuffling case (`state.slot === 0 && decisionSlot === 0`),
+      // `proposerShufflingDecisionRoot` returns `null` and we fall back to the canonical
+      // genesis root, because `head.blockRoot` is the current fork-choice head and may not
+      // equal the genesis root if the chain has advanced.
       const dependentRoot =
-        // In v2 the dependent root is different after fulu due to deterministic proposer lookahead
-        proposerShufflingDecisionRoot(opts?.v2 ? config.getForkName(startSlot) : ForkName.phase0, state, epoch) ||
-        (await getGenesisBlockRoot(state));
+        proposerShufflingDecisionRoot(
+          opts?.v2 ? config.getForkName(startSlot) : ForkName.phase0,
+          state,
+          epoch,
+          fromHex(head.blockRoot)
+        ) ?? (await getGenesisBlockRoot(state));
 
       return {
         data: duties,
diff --git a/packages/beacon-node/test/unit/api/impl/validator/duties/proposer.test.ts b/packages/beacon-node/test/unit/api/impl/validator/duties/proposer.test.ts
index b389bbb6ca15..0069a0bd66dc 100644
--- a/packages/beacon-node/test/unit/api/impl/validator/duties/proposer.test.ts
+++ b/packages/beacon-node/test/unit/api/impl/validator/duties/proposer.test.ts
@@ -107,6 +107,23 @@ describe("get proposers api impl", () => {
     );
   });
 
+  // Regression for the V1 path: pre-Fulu decision-slot logic asks for the block root at
+  // `startSlot(nextEpoch) - 1`, which is in the future relative to a mid-epoch head state.
+  // The dep_root must fall back to the head block root instead of throwing.
+  it("should get proposers for next epoch via V1 from a mid-epoch head state", async () => {
+    const nextEpoch = currentEpoch + 1;
+    const {data: result, meta} = (await api.getProposerDuties({epoch: nextEpoch})) as {
+      data: routes.validator.ProposerDutyList;
+      meta: {dependentRoot: string};
+    };
+
+    expect(result.length).toBe(SLOTS_PER_EPOCH);
+    expect(meta.dependentRoot).toBe(zeroProtoBlock.blockRoot);
+    expect(result.map((p) => p.slot)).toEqual(
+      Array.from({length: SLOTS_PER_EPOCH}, (_, i) => nextEpoch * SLOTS_PER_EPOCH + i)
+    );
+  });
+
   it("should get proposers for historical epoch", async () => {
     const historicalEpoch = currentEpoch - 2;
     initializeState(currentSlot - 2 * SLOTS_PER_EPOCH + 1);
diff --git a/packages/state-transition/src/util/shuffling.ts b/packages/state-transition/src/util/shuffling.ts
index 9710b2b3bf07..440414733a04 100644
--- a/packages/state-transition/src/util/shuffling.ts
+++ b/packages/state-transition/src/util/shuffling.ts
@@ -21,18 +21,32 @@ import {EpochShuffling} from "./epochShuffling.js";
  * Computed for the requested epoch, not `state.epoch`, so it is correct when `state` is one
  * epoch off the requested epoch (e.g. serving next-epoch duties from the current state).
  *
- * Returns `null` when the genesis block decides its own shuffling (caller falls back to the
- * genesis block root).
+ * `headBlockRoot` is the canonical head block root applied to `state`. When the decision
+ * slot is at or after `state.slot` (e.g. serving pre-Fulu `currentEpoch + 1` duties from
+ * a mid-epoch head state), the head block root is returned as the dependent root. This
+ * matches the beacon-API V1 rule of using the latest block applied to state when the
+ * decision slot is not yet in `block_roots`, and aligns with Lighthouse's
+ * `proposer_shuffling_decision_root_at_epoch` behavior.
+ *
+ * Returns `null` for the genesis-decides-its-own-shuffling case (`state.slot === 0 &&
+ * decisionSlot === 0`); the caller must fall back to the canonical genesis block root
+ * (typically via `getGenesisBlockRoot(state)`), because `headBlockRoot` may not equal
+ * the genesis root when the chain has advanced and we are serving epoch-0 duties from a
+ * loaded genesis state.
  */
 export function proposerShufflingDecisionRoot(
   fork: ForkName,
   state: IBeaconStateView,
-  proposalEpoch: Epoch
+  proposalEpoch: Epoch,
+  headBlockRoot: Root
 ): Root | null {
   const decisionSlot = proposerShufflingDecisionSlot(fork, proposalEpoch);
-  if (state.slot === decisionSlot) {
+  if (state.slot === 0 && decisionSlot === 0) {
     return null;
   }
+  if (state.slot <= decisionSlot) {
+    return headBlockRoot;
+  }
   return state.getBlockRootAtSlot(decisionSlot);
 }