diff --git a/eth/_utils/headers.py b/eth/_utils/headers.py
index 98b8cb94bb..c9bfa21bc9 100644
--- a/eth/_utils/headers.py
+++ b/eth/_utils/headers.py
@@ -4,10 +4,7 @@
     Tuple,
 )
 
-from eth_typing import (
-    Address,
-)
-
+from eth_typing import Address
 from eth.abc import BlockHeaderAPI
 from eth.constants import (
     BLANK_ROOT_HASH,
@@ -21,6 +18,7 @@
     GAS_LIMIT_USAGE_ADJUSTMENT_DENOMINATOR,
     ZERO_ADDRESS,
 )
+from eth.exceptions import PyEVMError
 from eth.typing import (
     BlockNumber,
     HeaderParams,
@@ -57,6 +55,7 @@ def fill_header_params_from_parent(
         gas_limit: int,
         difficulty: int,
         timestamp: int,
+        block_number: int = None,
         coinbase: Address = ZERO_ADDRESS,
         nonce: bytes = None,
         extra_data: bytes = None,
@@ -67,11 +66,13 @@ def fill_header_params_from_parent(
 
     if parent is None:
         parent_hash = GENESIS_PARENT_HASH
-        block_number = GENESIS_BLOCK_NUMBER
+        block_number = block_number if block_number else GENESIS_BLOCK_NUMBER
         if state_root is None:
             state_root = BLANK_ROOT_HASH
     else:
         parent_hash = parent.hash
+        if block_number:
+            raise PyEVMError("block_number cannot be configured if a parent header exists.")
         block_number = BlockNumber(parent.block_number + 1)
 
         if state_root is None:
diff --git a/tests/core/vm/test_vm.py b/tests/core/vm/test_vm.py
index 951c557fc6..efee5becf8 100644
--- a/tests/core/vm/test_vm.py
+++ b/tests/core/vm/test_vm.py
@@ -11,10 +11,13 @@
     MiningChain,
 )
 from eth.chains.mainnet import MAINNET_VMS
+from eth.exceptions import PyEVMError
 from eth.tools.builder.chain import api
 from eth.tools.factories.transaction import (
     new_transaction
 )
+from eth_typing import BlockNumber
+from eth._utils.headers import fill_header_params_from_parent
 
 
 @pytest.fixture(params=MAINNET_VMS)
@@ -191,3 +194,55 @@ def test_validate_gas_limit_too_high(noproof_consensus_chain):
 
     with pytest.raises(ValidationError, match="[Gg]as limit"):
         vm.validate_header(invalid_header, block1.header)
+
+
+@pytest.mark.parametrize(
+    "custom_header_params,null_parent",
+    (
+        ({
+            'gas_limit': 1,
+            'difficulty': 10,
+            'timestamp': 100,
+            'block_number': 1000
+        }, True),
+        ({
+            'gas_limit': 1,
+            'difficulty': 10,
+            'timestamp': 100,
+        }, False),
+        ({
+            'gas_limit': 1,
+            'difficulty': 10,
+            'timestamp': 100,
+            'block_number': 1000,
+        }, False)
+    )
+)
+def test_fill_header_params_from_parent(custom_header_params, null_parent,
+                                        noproof_consensus_chain):
+    # Handle cases which want to specify a null parent.
+    block = noproof_consensus_chain.mine_block()
+    header = block.header if null_parent is False else None
+
+    # Cannot specify block number and a parent.
+    if 'block_number' in custom_header_params and header is not None:
+        with pytest.raises(PyEVMError, match="block_number cannot be configured if a parent header exists."):
+            new_header_params = fill_header_params_from_parent(header, **custom_header_params)
+        return
+    new_header_params = fill_header_params_from_parent(header, **custom_header_params)
+
+    # Compare fields which are copied no matter what.
+    trivial_fields = ['gas_limit', 'difficulty', 'timestamp']
+    for field in trivial_fields:
+        assert new_header_params[field] == custom_header_params[field]
+
+    # Check `block_number` and `parent_hash` cases.
+    if 'block_number' in custom_header_params:
+        assert new_header_params['block_number'] == custom_header_params['block_number']
+        assert new_header_params['parent_hash'] == constants.GENESIS_PARENT_HASH
+    elif header is None:
+        assert new_header_params['block_number'] == constants.GENESIS_BLOCK_NUMBER
+        assert new_header_params['parent_hash'] == constants.GENESIS_PARENT_HASH
+    else:
+        assert new_header_params['block_number'] == BlockNumber(header['block_number'] + 1)
+        assert new_header_params['parent_hash'] == header.hash