diff --git a/src/ethereum/prague/fork.py b/src/ethereum/prague/fork.py
index 71f02cc0e2..be7472bf03 100644
--- a/src/ethereum/prague/fork.py
+++ b/src/ethereum/prague/fork.py
@@ -41,7 +41,6 @@
     increment_nonce,
     process_withdrawal,
     set_account_balance,
-    set_storage,
     state_root,
 )
 from .transactions import (
@@ -204,13 +203,6 @@ def state_transition(chain: BlockChain, block: Block) -> None:
     if block.ommers != ():
         raise InvalidBlock
 
-    set_storage(
-        chain.state,
-        HISTORY_STORAGE_ADDRESS,
-        ((block.header.number - 1) % HISTORY_SERVE_WINDOW).to_be_bytes32(),
-        U256.from_be_bytes(block.header.parent_hash),
-    )
-
     apply_body_output = apply_body(
         chain.state,
         get_last_256_block_hashes(chain),
@@ -728,6 +720,21 @@ def apply_body(
         excess_blob_gas,
     )
 
+    process_system_transaction(
+        HISTORY_STORAGE_ADDRESS,
+        block_hashes[-1],  # The parent hash
+        block_hashes,
+        coinbase,
+        block_number,
+        base_fee_per_gas,
+        block_gas_limit,
+        block_time,
+        prev_randao,
+        state,
+        chain_id,
+        excess_blob_gas,
+    )
+
     for i, tx in enumerate(map(decode_transaction, transactions)):
         trie_set(
             transactions_trie, rlp.encode(Uint(i)), encode_transaction(tx)
diff --git a/src/ethereum_spec_tools/evm_tools/t8n/__init__.py b/src/ethereum_spec_tools/evm_tools/t8n/__init__.py
index da13689085..5ac44d9b84 100644
--- a/src/ethereum_spec_tools/evm_tools/t8n/__init__.py
+++ b/src/ethereum_spec_tools/evm_tools/t8n/__init__.py
@@ -316,20 +316,27 @@ def apply_body(self) -> None:
         receipts_trie = self.fork.Trie(secured=False, default=None)
         block_logs = ()
         blob_gas_used = Uint(0)
-        if self.fork.is_after_fork("ethereum.prague"):
+        if (
+            self.fork.is_after_fork("ethereum.prague")
+            and not self.options.state_test
+        ):
             requests_trie = self.fork.Trie(secured=False, default=None)
             requests_from_execution: Tuple[Bytes, ...] = ()
 
-            if not self.options.state_test:
-                self.fork.set_storage(
-                    self.alloc.state,
-                    self.fork.HISTORY_STORAGE_ADDRESS,
-                    (
-                        (self.env.block_number - 1)
-                        % self.fork.HISTORY_SERVE_WINDOW
-                    ).to_be_bytes32(),
-                    U256.from_be_bytes(self.env.parent_hash),
-                )
+            self.fork.process_system_transaction(
+                self.fork.HISTORY_SERVE_WINDOW,
+                self.env.parent_hash,
+                self.env.block_hashes,
+                self.env.coinbase,
+                self.env.block_number,
+                self.env.base_fee_per_gas,
+                self.env.block_gas_limit,
+                self.env.block_timestamp,
+                self.env.prev_randao,
+                self.alloc.state,
+                self.chain_id,
+                self.env.excess_blob_gas,
+            )
 
         if (
             self.fork.is_after_fork("ethereum.cancun")
diff --git a/tests/prague/test_state_transition.py b/tests/prague/test_state_transition.py
index ce51c13099..ef4f1bcd98 100644
--- a/tests/prague/test_state_transition.py
+++ b/tests/prague/test_state_transition.py
@@ -105,6 +105,7 @@
     "tests/fixtures/latest_fork_tests/blockchain_tests/prague/eip7251_consolidations",
     "tests/fixtures/latest_fork_tests/blockchain_tests/prague/eip7685_general_purpose_el_requests",
     "tests/fixtures/latest_fork_tests/blockchain_tests/prague/eip2537_bls_12_381_precompiles",
+    "tests/fixtures/latest_fork_tests/blockchain_tests/prague/eip2935_historical_block_hashes_from_state",
     # TODO: Current test fixtures don't support EOF along with other
     # EIPs. This will be fixed in the future.
 )