diff --git a/core/state_processor.go b/core/state_processor.go
index 0bcdcc4260..486e12ab40 100644
--- a/core/state_processor.go
+++ b/core/state_processor.go
@@ -81,7 +81,12 @@ func (p *StateProcessor) Process(block *types.Block, statedb *state.StateDB, cfg
 		ProcessBeaconBlockRoot(*beaconRoot, vmenv, statedb)
 	}
 	if p.config.IsPrague(block.Number(), block.Time()) {
-		ProcessParentBlockHash(statedb, block.NumberU64()-1, block.ParentHash())
+		parent := p.bc.GetBlockByHash(block.ParentHash())
+		if !p.config.IsPrague(parent.Number(), parent.Time()) {
+			InsertBlockHashHistoryAtEip2935Fork(statedb, block.NumberU64()-1, block.ParentHash(), p.bc)
+		} else {
+			ProcessParentBlockHash(statedb, block.NumberU64()-1, block.ParentHash())
+		}
 	}
 	// Iterate over and process the individual transactions
 	for i, tx := range block.Transactions() {
@@ -194,6 +199,17 @@ func ProcessBeaconBlockRoot(beaconRoot common.Hash, vmenv *vm.EVM, statedb *stat
 	statedb.Finalise(true)
 }
 
+// InsertBlockHashHistoryAtEip2935Fork inserts the block hashes for the 256 ancestors
+// of the fork block.
+func InsertBlockHashHistoryAtEip2935Fork(statedb *state.StateDB, prevNumber uint64, prevHash common.Hash, chain consensus.ChainHeaderReader) {
+	ancestor := chain.GetHeader(prevHash, prevNumber)
+	for i := prevNumber; i > 0 && i >= prevNumber-256; i-- {
+		ProcessParentBlockHash(statedb, i, ancestor.Hash())
+		ancestor = chain.GetHeader(ancestor.ParentHash, ancestor.Number.Uint64()-1)
+	}
+}
+
+// ProcessParentBlockHash inserts the parent block hash into the history storage contract.
 func ProcessParentBlockHash(statedb *state.StateDB, prevNumber uint64, prevHash common.Hash) {
 	var key common.Hash
 	binary.BigEndian.PutUint64(key[24:], prevNumber)
diff --git a/core/vm/instructions.go b/core/vm/instructions.go
index 5a2b0fc4ab..bf21b8363d 100644
--- a/core/vm/instructions.go
+++ b/core/vm/instructions.go
@@ -449,22 +449,9 @@ func opBlockhash(pc *uint64, interpreter *EVMInterpreter, scope *ScopeContext) (
 	}
 
 	evm := interpreter.evm
-	bnum := evm.Context.BlockNumber.Uint64()
-	// if Prague is active, check if we are past the 256th block so that
-	// reading from the contract can be activated (EIP 2935).
-	if interpreter.evm.chainRules.IsPrague && bnum > 256 {
-		if getBlockHashFromContract(bnum-256, evm.StateDB) != (common.Hash{}) {
-			// EIP-2935 case: get the block number from the fork, as we are 256 blocks
-			// after the fork activation.
-
-			num.SetBytes(getBlockHashFromContract(num64, evm.StateDB).Bytes())
-			return nil, nil
-		}
-
-		// if the 256th ancestor didn't have its hash stored in the
-		// history contract, then we are within 256 blocks of the
-		// fork activation, and the former behavior should be retained.
-		// Fall through the legacy use case.
+	if evm.chainRules.IsPrague {
+		num.SetBytes(getBlockHashFromContract(num64, evm.StateDB).Bytes())
+		return nil, nil
 	}
 
 	var upper, lower uint64
diff --git a/core/vm/instructions_test.go b/core/vm/instructions_test.go
index 5f481a7fbe..bcbf08b4a4 100644
--- a/core/vm/instructions_test.go
+++ b/core/vm/instructions_test.go
@@ -827,27 +827,29 @@ func TestBlockHashEip2935(t *testing.T) {
 			TerminalTotalDifficulty:       big.NewInt(0),
 			TerminalTotalDifficultyPassed: true,
 		}
-		env             = NewEVM(blockContext, TxContext{}, statedb, chainConfig, Config{})
-		stack           = newstack()
-		pc              = uint64(0)
-		evmInterpreter  = env.interpreter
-		callBlockHash10 = func(t *testing.T, name string) {
-			stack.push(uint256.NewInt(10))
-			opBlockhash(&pc, evmInterpreter, &ScopeContext{nil, stack, nil})
-			if len(stack.data) != 1 {
-				t.Errorf("Expected one item on stack got %d: ", len(stack.data))
-			}
-			actual := stack.pop()
-			expected, overflow := uint256.FromBig(new(big.Int).SetBytes(expect.Bytes()))
-			if overflow {
-				t.Errorf("invalid overflow")
-			}
-			if actual.Cmp(expected) != 0 {
-				t.Errorf("%s: expected  %x, got %x", name, expected, actual)
+		env            = NewEVM(blockContext, TxContext{}, statedb, chainConfig, Config{})
+		stack          = newstack()
+		pc             = uint64(0)
+		evmInterpreter = env.interpreter
+		callBlockHashN = func(n uint64) func(t *testing.T, name string) uint256.Int {
+			return func(t *testing.T, name string) uint256.Int {
+				stack.push(uint256.NewInt(n))
+				opBlockhash(&pc, evmInterpreter, &ScopeContext{nil, stack, nil})
+				if len(stack.data) != 1 {
+					t.Errorf("Expected one item on stack got %d: ", len(stack.data))
+				}
+				return stack.pop()
 			}
 		}
+		callBlockHash10   = callBlockHashN(10)
+		callBlockHash1024 = callBlockHashN(1024)
 	)
 
+	expected, overflow := uint256.FromBig(new(big.Int).SetBytes(expect.Bytes()))
+	if overflow {
+		t.Errorf("invalid overflow")
+	}
+
 	// insert 500 block hashes, starting from genesis.
 	for i := uint64(0); i < 500; i++ {
 		var blockNumber common.Hash
@@ -857,12 +859,24 @@ func TestBlockHashEip2935(t *testing.T) {
 
 	// simulate a call to BLOCKHASH at block 100, i.e. less than 256
 	// blocks after a genesis with eip 2935 activated.
-	callBlockHash10(t, "legacy")
+	actual := callBlockHash10(t, "legacy")
+	if actual.Cmp(expected) != 0 {
+		t.Errorf("%s: expected  %x, got %x", "legacy", expected, actual)
+	}
 
 	// now do the same thing much later, after all blocks have
 	// been inserted.
-	env.Context.BlockNumber.SetInt64(500)
-	callBlockHash10(t, "contract")
+	env.Context.BlockNumber.SetInt64(501)
+	actual = callBlockHash10(t, "contract")
+	if actual.Cmp(expected) != 0 {
+		t.Errorf("%s: expected  %x, got %x", "contract", expected, actual)
+	}
+
+	// still at block 501, but now request the hash of a higher block
+	actual = callBlockHash1024(t, "contract with non-existent block hash")
+	if !actual.IsZero() {
+		t.Errorf("%s: expected  0, got %x", "contract with non-existent block hash", actual)
+	}
 }
 
 func TestOpMCopy(t *testing.T) {