diff --git a/cmd/evm/internal/t8ntool/execution.go b/cmd/evm/internal/t8ntool/execution.go
index 8c6725cb316b..5847f6f2a534 100644
--- a/cmd/evm/internal/t8ntool/execution.go
+++ b/cmd/evm/internal/t8ntool/execution.go
@@ -184,6 +184,7 @@ func (pre *Prestate) Apply(vmConfig vm.Config, chainConfig *params.ChainConfig,
 		misc.ApplyDAOHardFork(statedb)
 	}
 	if chainConfig.IsPrague(big.NewInt(int64(pre.Env.Number)), pre.Env.Timestamp) {
+		// XXX figure out what to do for older hashes?
 		core.ProcessParentBlockHash(statedb, pre.Env.Number-1, *pre.Env.ParentHash)
 	}
 	var blobGasUsed uint64
diff --git a/core/chain_makers.go b/core/chain_makers.go
index 37a5fbf5100f..5b9dc0c6ff08 100644
--- a/core/chain_makers.go
+++ b/core/chain_makers.go
@@ -386,7 +386,12 @@ func GenerateVerkleChain(config *params.ChainConfig, parent *types.Block, engine
 		fmt.Println("prestate", preState.GetTrie().(*trie.VerkleTrie).ToDot())
 
 		if config.IsPrague(b.header.Number, b.header.Time) {
-			ProcessParentBlockHash(statedb, b.header.Number.Uint64()-1, b.header.ParentHash)
+			if !config.IsPrague(b.parent.Number(), b.parent.Time()) {
+				// Transition case: insert all 256 ancestors
+				InsertBlockHashHistoryAtEip2935Fork(statedb, b.header.Number.Uint64()-1, b.header.ParentHash, chainreader)
+			} else {
+				ProcessParentBlockHash(statedb, b.header.Number.Uint64()-1, b.header.ParentHash)
+			}
 		}
 
 		// Mutate the state and block according to any hard-fork specs
diff --git a/core/state_processor.go b/core/state_processor.go
index b22c45469e6f..daf2bb729fc4 100644
--- a/core/state_processor.go
+++ b/core/state_processor.go
@@ -87,7 +87,12 @@ func (p *StateProcessor) Process(block *types.Block, statedb *state.StateDB, cfg
 		signer  = types.MakeSigner(p.config, header.Number, header.Time)
 	)
 	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() {
@@ -364,6 +369,14 @@ func (kvm *keyValueMigrator) migrateCollectedKeyValues(tree *trie.VerkleTrie) er
 	return nil
 }
 
+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())
+	}
+}
+
 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 00787b3d030f..29e3022fea0e 100644
--- a/core/vm/instructions.go
+++ b/core/vm/instructions.go
@@ -515,22 +515,10 @@ 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 evm.chainRules.IsPrague && bnum > 256 {
-		if getBlockHashFromContract(bnum-256, evm.StateDB, evm.Accesses) != (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, evm.Accesses).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 Prague is active, read it from the history contract (EIP 2935).
+	if evm.chainRules.IsPrague {
+		num.SetBytes(getBlockHashFromContract(num64, evm.StateDB, evm.Accesses).Bytes())
+		return nil, nil
 	}
 
 	var upper, lower uint64
diff --git a/miner/worker.go b/miner/worker.go
index ef8d6087b7cd..aae4fe8b6454 100644
--- a/miner/worker.go
+++ b/miner/worker.go
@@ -921,7 +921,12 @@ func (w *worker) prepareWork(genParams *generateParams) (*environment, error) {
 		return nil, err
 	}
 	if w.chainConfig.IsPrague(header.Number, header.Time) {
-		core.ProcessParentBlockHash(env.state, header.Number.Uint64()-1, header.ParentHash)
+		parent := w.chain.GetHeaderByNumber(header.Number.Uint64() - 1)
+		if !w.chain.Config().IsPrague(parent.Number, parent.Time) {
+			core.InsertBlockHashHistoryAtEip2935Fork(env.state, header.Number.Uint64()-1, header.ParentHash, w.chain)
+		} else {
+			core.ProcessParentBlockHash(env.state, header.Number.Uint64()-1, header.ParentHash)
+		}
 	}
 	return env, nil
 }