diff --git a/consensus/proto_array/src/error.rs b/consensus/proto_array/src/error.rs
index bb5eea569d..bb47af97d9 100644
--- a/consensus/proto_array/src/error.rs
+++ b/consensus/proto_array/src/error.rs
@@ -61,6 +61,7 @@ pub enum Error {
         block_root: Hash256,
     },
     NoViableChildren,
+    OnBlockRequiresProposerIndex,
 }
 
 impl From<ArithError> for Error {
diff --git a/consensus/proto_array/src/fork_choice_test_definition.rs b/consensus/proto_array/src/fork_choice_test_definition.rs
index 4507e013ba..b6ccc4d435 100644
--- a/consensus/proto_array/src/fork_choice_test_definition.rs
+++ b/consensus/proto_array/src/fork_choice_test_definition.rs
@@ -280,7 +280,7 @@ impl ForkChoiceTestDefinition {
                         unrealized_finalized_checkpoint: None,
                         execution_payload_parent_hash,
                         execution_payload_block_hash,
-                        proposer_index: None,
+                        proposer_index: Some(0),
                     };
                     fork_choice
                         .process_block::<MainnetEthSpec>(
diff --git a/consensus/proto_array/src/proto_array.rs b/consensus/proto_array/src/proto_array.rs
index e3671eef7d..374190f9ed 100644
--- a/consensus/proto_array/src/proto_array.rs
+++ b/consensus/proto_array/src/proto_array.rs
@@ -551,6 +551,12 @@ impl ProtoArray {
             return Ok(());
         }
 
+        // We do not allow `proposer_index=None` for calls to `on_block`, it is only non-optional
+        // for backwards-compatibility with pre-Gloas V17 proto nodes.
+        let Some(proposer_index) = block.proposer_index else {
+            return Err(Error::OnBlockRequiresProposerIndex);
+        };
+
         let node_index = self.nodes.len();
 
         let parent_index = block
@@ -658,7 +664,7 @@ impl ProtoArray {
                     BitVector::default()
                 },
                 payload_received: is_genesis,
-                proposer_index: block.proposer_index.unwrap_or(0),
+                proposer_index,
                 // Spec: `record_block_timeliness` + `get_forkchoice_store`.
                 // Anchor gets [True, True]. Others computed from time_into_slot.
                 block_timeliness_attestation_threshold: is_genesis
diff --git a/consensus/proto_array/src/proto_array_fork_choice.rs b/consensus/proto_array/src/proto_array_fork_choice.rs
index 94660f24ff..e8ad6c063a 100644
--- a/consensus/proto_array/src/proto_array_fork_choice.rs
+++ b/consensus/proto_array/src/proto_array_fork_choice.rs
@@ -492,7 +492,7 @@ impl ProtoArrayForkChoice {
             unrealized_finalized_checkpoint: Some(finalized_checkpoint),
             execution_payload_parent_hash,
             execution_payload_block_hash,
-            proposer_index: None,
+            proposer_index: Some(0),
         };
 
         proto_array
@@ -1338,7 +1338,7 @@ mod test_compute_deltas {
                     unrealized_finalized_checkpoint: Some(genesis_checkpoint),
                     execution_payload_parent_hash: None,
                     execution_payload_block_hash: None,
-                    proposer_index: None,
+                    proposer_index: Some(0),
                 },
                 genesis_slot + 1,
                 genesis_checkpoint,
@@ -1368,7 +1368,7 @@ mod test_compute_deltas {
                     unrealized_finalized_checkpoint: None,
                     execution_payload_parent_hash: None,
                     execution_payload_block_hash: None,
-                    proposer_index: None,
+                    proposer_index: Some(0),
                 },
                 genesis_slot + 1,
                 genesis_checkpoint,
@@ -1505,7 +1505,7 @@ mod test_compute_deltas {
                         unrealized_finalized_checkpoint: Some(genesis_checkpoint),
                         execution_payload_parent_hash: None,
                         execution_payload_block_hash: None,
-                        proposer_index: None,
+                        proposer_index: Some(0),
                     },
                     Slot::from(block.slot),
                     genesis_checkpoint,