diff --git a/packages/beacon-node/src/api/impl/validator/index.ts b/packages/beacon-node/src/api/impl/validator/index.ts
index ea94cb4b49f7..3e193aef47b2 100644
--- a/packages/beacon-node/src/api/impl/validator/index.ts
+++ b/packages/beacon-node/src/api/impl/validator/index.ts
@@ -1207,7 +1207,10 @@ export function getValidatorApi(
       const isPostFulu = isForkPostFulu(config.getForkName(startSlot));
       const maxFutureEpoch = isPostFulu && nearNextEpoch && opts?.v2 ? nextEpoch + 1 : nextEpoch;
       if (currentEpoch >= 0 && epoch > maxFutureEpoch) {
-        throw new ApiError(400, `Requested epoch ${epoch} must not be more than one epoch in the future`);
+        throw new ApiError(
+          400,
+          `Requested epoch ${epoch} must not be more than ${maxFutureEpoch}, currentEpoch=${currentEpoch}, v2=${opts?.v2 ?? false}`
+        );
       }
 
       const head = chain.forkChoice.getHead();
@@ -1291,17 +1294,35 @@ 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.
-      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));
+      // In v2 the dependent root is different after fulu due to deterministic proposer lookahead
+      let dependentRoot = proposerShufflingDecisionRoot(
+        opts?.v2 ? config.getForkName(startSlot) : ForkName.phase0,
+        state,
+        epoch
+      );
+      const logCtx = {
+        epoch,
+        stateSlot: state.slot,
+        stateEpoch: state.epoch,
+        v2: opts?.v2 ?? false,
+      };
+      if (dependentRoot === null) {
+        // fallback to get_proposer_duties() v1, also in lodestar v1.43
+        logger.verbose("Proposer duties decision root not in state, falling back to state epoch", logCtx);
+        dependentRoot = proposerShufflingDecisionRoot(ForkName.phase0, state, state.epoch);
+      }
+      if (dependentRoot === null) {
+        logger.verbose("Proposer duties decision root not in state, falling back to genesis block root", logCtx);
+        dependentRoot = await getGenesisBlockRoot(state);
+      }
+
+      const dependentRootHex = toRootHex(dependentRoot);
+      logger.verbose("Computed proposer duties decision root", {...logCtx, dependentRoot: dependentRootHex});
 
       return {
         data: duties,
         meta: {
-          dependentRoot: toRootHex(dependentRoot),
+          dependentRoot: dependentRootHex,
           executionOptimistic: isOptimisticBlock(head),
         },
       };
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..82eb0485847c 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
@@ -4,6 +4,7 @@ import {getConfig} from "@lodestar/config/test-utils";
 import {ForkName, MAX_EFFECTIVE_BALANCE, SLOTS_PER_EPOCH} from "@lodestar/params";
 import {BeaconStateAllForks, BeaconStateView} from "@lodestar/state-transition";
 import {Slot} from "@lodestar/types";
+import {toRootHex} from "@lodestar/utils";
 import {SYNC_TOLERANCE_EPOCHS, getValidatorApi} from "../../../../../../src/api/impl/validator/index.js";
 import {defaultApiOptions} from "../../../../../../src/api/options.js";
 import {FAR_FUTURE_EPOCH} from "../../../../../../src/constants/index.js";
@@ -107,6 +108,31 @@ describe("get proposers api impl", () => {
     );
   });
 
+  // Regression #9380: v1 getProposerDuties for next epoch must not throw on the dependent root.
+  // The requested-epoch decision slot is the last slot of the current epoch (in the future for a
+  // head state), so it falls back to the state-epoch decision root (last block of previous epoch),
+  // which is stable and, post-Fulu, identical to v2.
+  it("should get v1 proposers for next epoch with stable dependent root", async () => {
+    const nextEpoch = currentEpoch + 1;
+    const v1 = (await api.getProposerDuties({epoch: nextEpoch})) as {meta: {dependentRoot: string}};
+    const v2 = (await api.getProposerDutiesV2({epoch: nextEpoch})) as {meta: {dependentRoot: string}};
+
+    const expected = toRootHex(new BeaconStateView(cachedState).getBlockRootAtSlot(currentSlot - 1));
+    expect(v1.meta.dependentRoot).toBe(expected);
+    expect(v2.meta.dependentRoot).toBe(expected);
+  });
+
+  it("should get v1 proposers for next epoch from a mid-epoch head state", async () => {
+    vi.advanceTimersByTime(15 * config.SLOT_DURATION_MS);
+    initializeState(currentSlot + 15);
+    modules.chain.getHeadStateAtCurrentEpoch.mockResolvedValue(new BeaconStateView(cachedState));
+
+    const v1 = (await api.getProposerDuties({epoch: currentEpoch + 1})) as {meta: {dependentRoot: string}};
+
+    const expected = toRootHex(new BeaconStateView(cachedState).getBlockRootAtSlot(currentSlot - 1));
+    expect(v1.meta.dependentRoot).toBe(expected);
+  });
+
   it("should get proposers for historical epoch", async () => {
     const historicalEpoch = currentEpoch - 2;
     initializeState(currentSlot - 2 * SLOTS_PER_EPOCH + 1);
@@ -129,7 +155,7 @@ describe("get proposers api impl", () => {
 
   it("should raise error for more than one epoch in the future", async () => {
     await expect(api.getProposerDutiesV2({epoch: currentEpoch + 2})).rejects.toThrow(
-      "Requested epoch 4 must not be more than one epoch in the future"
+      "Requested epoch 4 must not be more than 3, currentEpoch=2, v2=true"
     );
   });
 
diff --git a/packages/state-transition/src/util/shuffling.ts b/packages/state-transition/src/util/shuffling.ts
index 9710b2b3bf07..9636821be020 100644
--- a/packages/state-transition/src/util/shuffling.ts
+++ b/packages/state-transition/src/util/shuffling.ts
@@ -21,8 +21,8 @@ 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).
+ * Returns `null` when the decision block is not in the state's past (the genesis block decides
+ * its own shuffling, or it has not been produced yet); caller supplies the fallback.
  */
 export function proposerShufflingDecisionRoot(
   fork: ForkName,
@@ -30,7 +30,8 @@ export function proposerShufflingDecisionRoot(
   proposalEpoch: Epoch
 ): Root | null {
   const decisionSlot = proposerShufflingDecisionSlot(fork, proposalEpoch);
-  if (state.slot === decisionSlot) {
+  // Return null when the decision block is not in the state's past or the getBlockRootAtSlot() api will throw
+  if (decisionSlot >= state.slot) {
     return null;
   }
   return state.getBlockRootAtSlot(decisionSlot);