diff --git a/server/api/ballot_manifest.py b/server/api/ballot_manifest.py
index fdca19358..1b35dd9ac 100644
--- a/server/api/ballot_manifest.py
+++ b/server/api/ballot_manifest.py
@@ -120,15 +120,13 @@ def process() -> None:
             AuditType.HYBRID,
         ]
 
-        is_counting_group_required = is_enabled_sample_extra_batches_by_counting_group(
-            jurisdiction.election
-        )
-
         columns = [
             CSVColumnType(
                 CONTAINER,
                 CSVValueType.TEXT,
-                required_column=is_counting_group_required,
+                # Optionally, users can include a "Container" column to help
+                # identify ballots in different storage locations.
+                required_column=False,
             ),
             CSVColumnType(
                 TABULATOR,
@@ -151,6 +149,9 @@ def process() -> None:
         validate_is_not_batch_inventory_worksheet(manifest_file)
         manifest_csv = parse_csv(manifest_file, columns)
 
+        is_counting_group_required = is_enabled_sample_extra_batches_by_counting_group(
+            jurisdiction.election
+        )
         counting_group_allowlist = [item.value for item in CountingGroup]
         counting_group_allowset = set(counting_group_allowlist)
 
@@ -158,14 +159,21 @@ def process() -> None:
         num_ballots = 0
 
         for row_index, row in enumerate(manifest_csv):
-            counting_group = row.get(CONTAINER, None)
-            if (
-                is_counting_group_required
-                and not counting_group in counting_group_allowset
-            ):
-                raise CSVParseError(
-                    f"Invalid value for column \"Container\", row {row_index+2}: \"{counting_group}\". Use the Batch Audit File Preparation Tool to create your ballot manifest, or correct this value to one of the following: {', '.join(counting_group_allowlist)}."
-                )
+            # For the "sample extra batches by counting group" feature, we
+            # require the Container column to identify the counting group, so we
+            # validate it here. We want to provide special custom error
+            # messages, so we don't use the built-in "required_column" option in
+            # CSVColumnType.
+            if is_counting_group_required:
+                if CONTAINER not in row:
+                    raise CSVParseError(
+                        'Missing required column "Container". Use the Batch Audit File Preparation Tool to create your ballot manifest.'
+                    )
+                counting_group = row.get(CONTAINER)
+                if counting_group not in counting_group_allowset:
+                    raise CSVParseError(
+                        f"Invalid value for column \"Container\", row {row_index+2}: \"{counting_group}\". Use the Batch Audit File Preparation Tool to create your ballot manifest, or correct this value to one of the following: {', '.join(counting_group_allowlist)}."
+                    )
 
             batch = Batch(
                 id=str(uuid.uuid4()),
diff --git a/server/tests/batch_comparison/test_sample_extra_batches_by_counting_group.py b/server/tests/batch_comparison/test_sample_extra_batches_by_counting_group.py
index 309a11896..3faf8c741 100644
--- a/server/tests/batch_comparison/test_sample_extra_batches_by_counting_group.py
+++ b/server/tests/batch_comparison/test_sample_extra_batches_by_counting_group.py
@@ -567,3 +567,34 @@ def test_sample_extra_batches_with_invalid_counting_group(
             },
         },
     )
+
+    # Missing the "Container" column
+    set_logged_in_user(
+        client, UserType.JURISDICTION_ADMIN, default_ja_email(election_id)
+    )
+    rv = upload_ballot_manifest(
+        client,
+        io.BytesIO(b"Batch Name,Number of Ballots\n" b"Batch 1,500\n"),
+        election_id,
+        jurisdiction_ids[0],
+    )
+    assert_ok(rv)
+
+    rv = client.get(
+        f"/api/election/{election_id}/jurisdiction/{jurisdiction_ids[0]}/ballot-manifest"
+    )
+    compare_json(
+        json.loads(rv.data),
+        {
+            "file": {
+                "name": asserts_startswith("manifest"),
+                "uploadedAt": assert_is_date,
+            },
+            "processing": {
+                "status": ProcessingStatus.ERRORED,
+                "startedAt": assert_is_date,
+                "completedAt": assert_is_date,
+                "error": 'Missing required column "Container". Use the Batch Audit File Preparation Tool to create your ballot manifest.',
+            },
+        },
+    )