diff --git a/beacon_node/beacon_chain/src/block_verification.rs b/beacon_node/beacon_chain/src/block_verification.rs
index 1b0aea5a2f..9bb6757341 100644
--- a/beacon_node/beacon_chain/src/block_verification.rs
+++ b/beacon_node/beacon_chain/src/block_verification.rs
@@ -2148,11 +2148,13 @@ pub fn verify_header_signature<T: BeaconChainTypes, Err: BlockBlobError>(
         .get(header.message.proposer_index as usize)
         .cloned()
         .ok_or(Err::unknown_validator_error(header.message.proposer_index))?;
-    let head_fork = chain.canonical_head.cached_head().head_fork();
+    let fork = chain
+        .spec
+        .fork_at_epoch(header.message.slot.epoch(T::EthSpec::slots_per_epoch()));
 
     if header.verify_signature::<T::EthSpec>(
         &proposer_pubkey,
-        &head_fork,
+        &fork,
         chain.genesis_validators_root,
         &chain.spec,
     ) {
diff --git a/beacon_node/beacon_chain/src/canonical_head.rs b/beacon_node/beacon_chain/src/canonical_head.rs
index db071db166..1a08ac3f88 100644
--- a/beacon_node/beacon_chain/src/canonical_head.rs
+++ b/beacon_node/beacon_chain/src/canonical_head.rs
@@ -918,6 +918,13 @@ impl<T: BeaconChainTypes> BeaconChain<T> {
                 .start_slot(T::EthSpec::slots_per_epoch()),
         );
 
+        self.observed_column_sidecars.write().prune(
+            new_view
+                .finalized_checkpoint
+                .epoch
+                .start_slot(T::EthSpec::slots_per_epoch()),
+        );
+
         self.observed_slashable.write().prune(
             new_view
                 .finalized_checkpoint
diff --git a/beacon_node/beacon_chain/tests/column_verification.rs b/beacon_node/beacon_chain/tests/column_verification.rs
index ffbc460465..f048a08bb8 100644
--- a/beacon_node/beacon_chain/tests/column_verification.rs
+++ b/beacon_node/beacon_chain/tests/column_verification.rs
@@ -116,3 +116,96 @@ async fn rpc_columns_with_invalid_header_signature() {
         BlockError::InvalidSignature(InvalidSignature::ProposerSignature)
     ));
 }
+
+// Regression test for verify_header_signature bug: it uses head_fork() which is wrong for fork blocks
+#[tokio::test]
+async fn verify_header_signature_fork_block_bug() {
+    // Create a spec with all forks enabled at genesis except Fulu which is at epoch 1
+    // This allows us to easily create the scenario where the head is at Electra
+    // but we're trying to verify a block from Fulu epoch
+    let mut spec = test_spec::<E>();
+
+    // Only run this test for FORK_NAME=fulu.
+    if !spec.is_fulu_scheduled() || spec.is_gloas_scheduled() {
+        return;
+    }
+
+    spec.altair_fork_epoch = Some(Epoch::new(0));
+    spec.bellatrix_fork_epoch = Some(Epoch::new(0));
+    spec.capella_fork_epoch = Some(Epoch::new(0));
+    spec.deneb_fork_epoch = Some(Epoch::new(0));
+    spec.electra_fork_epoch = Some(Epoch::new(0));
+    let fulu_fork_epoch = Epoch::new(1);
+    spec.fulu_fork_epoch = Some(fulu_fork_epoch);
+
+    let spec = Arc::new(spec);
+    let harness = get_harness(VALIDATOR_COUNT, spec.clone(), NodeCustodyType::Supernode);
+    harness.execution_block_generator().set_min_blob_count(1);
+
+    // Add some blocks in epoch 0 (Electra)
+    harness
+        .extend_chain(
+            E::slots_per_epoch() as usize - 1,
+            BlockStrategy::OnCanonicalHead,
+            AttestationStrategy::AllValidators,
+        )
+        .await;
+
+    // Verify we're still in epoch 0 (Electra)
+    let pre_fork_state = harness.get_current_state();
+    assert_eq!(pre_fork_state.current_epoch(), Epoch::new(0));
+    assert!(matches!(pre_fork_state, BeaconState::Electra(_)));
+
+    // Now produce a block at the first slot of epoch 1 (Fulu fork).
+    // make_block will advance the state which will trigger the Electra->Fulu upgrade.
+    let fork_slot = fulu_fork_epoch.start_slot(E::slots_per_epoch());
+    let ((signed_block, opt_blobs), _state_root) =
+        harness.make_block(pre_fork_state.clone(), fork_slot).await;
+    let (_, blobs) = opt_blobs.expect("Blobs should be present");
+    assert!(!blobs.is_empty(), "Block should have blobs");
+    let block_root = signed_block.canonical_root();
+
+    // Process the block WITHOUT blobs to make it unavailable.
+    // The block will be accepted but won't become the head because it's not fully available.
+    // This keeps the head at the pre-fork state (Electra).
+    harness.advance_slot();
+    let rpc_block = harness
+        .build_rpc_block_from_blobs(block_root, signed_block.clone(), None)
+        .expect("Should build RPC block");
+    let availability = harness
+        .chain
+        .process_block(
+            block_root,
+            rpc_block,
+            NotifyExecutionLayer::Yes,
+            BlockImportSource::RangeSync,
+            || Ok(()),
+        )
+        .await
+        .expect("Block should be processed");
+    assert_eq!(
+        availability,
+        AvailabilityProcessingStatus::MissingComponents(fork_slot, block_root),
+        "Block should be pending availability"
+    );
+
+    // The head should still be in epoch 0 (Electra) because the fork block isn't available
+    let current_head_state = harness.get_current_state();
+    assert_eq!(current_head_state.current_epoch(), Epoch::new(0));
+    assert!(matches!(current_head_state, BeaconState::Electra(_)));
+
+    // Now try to process columns for the fork block.
+    // The bug: verify_header_signature previously used head_fork() which fetched the fork from
+    // the head state (still Electra fork), but the block was signed with the Fulu fork version.
+    // This caused an incorrect signature verification failure.
+    let data_column_sidecars =
+        generate_data_column_sidecars_from_block(&signed_block, &harness.chain.spec);
+
+    // Now that the bug is fixed, the block should import.
+    let status = harness
+        .chain
+        .process_rpc_custody_columns(data_column_sidecars)
+        .await
+        .unwrap();
+    assert_eq!(status, AvailabilityProcessingStatus::Imported(block_root));
+}