diff --git a/src/ape_ethereum/provider.py b/src/ape_ethereum/provider.py
index 32ab06f426..2c0010b231 100644
--- a/src/ape_ethereum/provider.py
+++ b/src/ape_ethereum/provider.py
@@ -25,6 +25,7 @@
     get_calltree_from_parity_trace,
 )
 from pydantic.dataclasses import dataclass
+from requests import HTTPError
 from web3 import HTTPProvider, IPCProvider, Web3
 from web3.exceptions import ContractLogicError as Web3ContractLogicError
 from web3.exceptions import (
@@ -1078,7 +1079,16 @@ def _create_trace_frame(self, evm_frame: EvmTraceFrame) -> TraceFrame:
 
     def _make_request(self, endpoint: str, parameters: Optional[List] = None) -> Any:
         parameters = parameters or []
-        result = self.web3.provider.make_request(RPCEndpoint(endpoint), parameters)
+
+        try:
+            result = self.web3.provider.make_request(RPCEndpoint(endpoint), parameters)
+        except HTTPError as err:
+            if "method not allowed" in str(err).lower():
+                raise APINotImplementedError(
+                    f"RPC method '{endpoint}' is not implemented by this node instance."
+                )
+
+            raise ProviderError(str(err)) from err
 
         if "error" in result:
             error = result["error"]
@@ -1419,7 +1429,11 @@ def get_call_tree(self, txn_hash: str) -> CallTreeNode:
         try:
             # Try the Parity traces first, in case node client supports it.
             tree = self._get_parity_call_tree(txn_hash)
-        except Exception:
+        except (ValueError, APINotImplementedError, ProviderError):
+            self.can_use_parity_traces = False
+            return self._get_geth_call_tree(txn_hash)
+        except Exception as err:
+            logger.error(f"Unknown exception while checking for Parity-trace support: {err} ")
             self.can_use_parity_traces = False
             return self._get_geth_call_tree(txn_hash)
 
diff --git a/tests/functional/test_provider.py b/tests/functional/test_provider.py
index c12432e5a2..6540c15a34 100644
--- a/tests/functional/test_provider.py
+++ b/tests/functional/test_provider.py
@@ -7,6 +7,7 @@
 from eth_typing import HexStr
 from eth_utils import ValidationError
 from hexbytes import HexBytes
+from requests import HTTPError
 from web3.exceptions import ContractPanicError
 
 from ape.exceptions import (
@@ -378,6 +379,28 @@ def custom_make_request(rpc, params):
         eth_tester_provider._make_request("ape_thisDoesNotExist")
 
 
+def test_make_request_handles_http_error_method_not_allowed(eth_tester_provider, mock_web3):
+    """
+    Simulate what *most* of the dev providers do, like hardhat, anvil, and ganache.
+    """
+    real_web3 = eth_tester_provider._web3
+    mock_web3.eth = real_web3.eth
+    eth_tester_provider._web3 = mock_web3
+
+    def custom_make_request(rpc, params):
+        if rpc == "ape_thisDoesNotExist":
+            raise HTTPError("Client error: Method Not Allowed")
+
+        return real_web3.provider.make_request(rpc, params)
+
+    mock_web3.provider.make_request.side_effect = custom_make_request
+    with pytest.raises(
+        APINotImplementedError,
+        match="RPC method 'ape_thisDoesNotExist' is not implemented by this node instance.",
+    ):
+        eth_tester_provider._make_request("ape_thisDoesNotExist")
+
+
 def test_base_fee(eth_tester_provider):
     actual = eth_tester_provider.base_fee
     assert actual > 0