diff --git a/jstests/multiVersion/long_index_mixed_version_replset.js b/jstests/multiVersion/long_index_mixed_version_replset.js
new file mode 100644
index 00000000000..b28ce5966c5
--- /dev/null
+++ b/jstests/multiVersion/long_index_mixed_version_replset.js
@@ -0,0 +1,47 @@
+/**
+ * Long index namespaces exceeding 127 characters are supported starting in 4.2.
+ * However, we should still disallow long index namespaces under FCV 4.0.
+ * TODO: remove this test in 4.4.
+ */
+(function() {
+    'use strict';
+
+    TestData.replSetFeatureCompatibilityVersion = '4.0';
+    const rst = new ReplSetTest({
+        nodes: [
+            {binVersion: 'latest'},
+            {rsConfig: {priority: 0, votes: 0}},
+        ]
+    });
+    rst.startSet();
+    rst.initiate();
+    rst.restart(1, {binVersion: '4.0'});
+
+    const primary = rst.getPrimary();
+    const mydb = primary.getDB('test');
+    const coll = mydb.getCollection('long_index_name');
+
+    // Compute maximum index name length for this collection under FCV 4.0.
+    const maxNsLength = 127;
+    const maxIndexNameLength = maxNsLength - (coll.getFullName() + ".$").length;
+    jsTestLog('Max index name length under FCV 4.0 = ' + maxIndexNameLength);
+
+    // Create an index with the longest name allowed for this collection.
+    assert.commandWorked(coll.createIndex({a: 1}, {name: 'a'.repeat(maxIndexNameLength)}));
+
+    // If this command succeeds unexpectedly, it will cause an fassert on the 4.0 secondary which
+    // cannot handle long index namespaces, with a "CannotCreateIndex: ... index name ... too long"
+    // error message.
+    assert.commandFailedWithCode(
+        coll.createIndex({b: 1}, {name: 'b'.repeat(maxIndexNameLength + 1)}),
+        ErrorCodes.CannotCreateIndex);
+
+    // The existing index on {x: 1} has an index name that is the longest supported under FCV 4.0
+    // for the current collection name.
+    // Any attempt to rename this collection with a longer name must fail. Otherwise, the invalid
+    // index namespace will cause the 4.0 secondary to fassert.
+    assert.commandFailedWithCode(coll.renameCollection(coll.getName() + 'z'),
+                                 ErrorCodes.InvalidLength);
+
+    rst.stopSet();
+})();
diff --git a/src/mongo/db/catalog/SConscript b/src/mongo/db/catalog/SConscript
index 97f4402ed92..7973ae3cccc 100644
--- a/src/mongo/db/catalog/SConscript
+++ b/src/mongo/db/catalog/SConscript
@@ -287,6 +287,7 @@ env.Library(
         '$BUILD_DIR/mongo/db/repl/drop_pending_collection_reaper',
         '$BUILD_DIR/mongo/db/repl/oplog',
         '$BUILD_DIR/mongo/db/s/balancer',
+        '$BUILD_DIR/mongo/db/server_options_core',
         '$BUILD_DIR/mongo/db/service_context',
         '$BUILD_DIR/mongo/db/storage/key_string',
         '$BUILD_DIR/mongo/db/system_index',
@@ -322,6 +323,7 @@ env.Library(
         '$BUILD_DIR/mongo/db/background',
         '$BUILD_DIR/mongo/db/db_raii',
         '$BUILD_DIR/mongo/db/query_exec',
+        '$BUILD_DIR/mongo/db/server_options_core',
         '$BUILD_DIR/mongo/db/views/views',
         '$BUILD_DIR/mongo/db/write_ops',
     ],
diff --git a/src/mongo/db/catalog/index_catalog_impl.cpp b/src/mongo/db/catalog/index_catalog_impl.cpp
index 22dad6daeac..8a3cbfc8f0f 100644
--- a/src/mongo/db/catalog/index_catalog_impl.cpp
+++ b/src/mongo/db/catalog/index_catalog_impl.cpp
@@ -620,8 +620,10 @@ Status IndexCatalogImpl::_isSpecOk(OperationContext* opCtx, const BSONObj& spec)
     // namespace length constraints as the ones in created by users.
     // Index names do not limit the maximum allowable length of the target namespace under FCV 4.2
     // and above.
-    // TODO(SERVER-35824): Re-enable index namespace check under FCV 4.0.
-    const bool checkIndexNamespace = false;
+    const auto checkIndexNamespace =
+        serverGlobalParams.featureCompatibility.isVersionInitialized() &&
+        serverGlobalParams.featureCompatibility.getVersion() !=
+            ServerGlobalParams::FeatureCompatibility::Version::kFullyUpgradedTo42;
     if (checkIndexNamespace && !nss.isDropPendingNamespace()) {
         auto indexNamespace = IndexDescriptor::makeIndexNamespace(nss.ns(), name);
         if (indexNamespace.length() > NamespaceString::MaxNsLen)
diff --git a/src/mongo/db/catalog/rename_collection.cpp b/src/mongo/db/catalog/rename_collection.cpp
index fcd24ad99d2..deccc82ce9b 100644
--- a/src/mongo/db/catalog/rename_collection.cpp
+++ b/src/mongo/db/catalog/rename_collection.cpp
@@ -51,6 +51,7 @@
 #include "mongo/db/repl/replication_coordinator.h"
 #include "mongo/db/s/collection_sharding_state.h"
 #include "mongo/db/s/database_sharding_state.h"
+#include "mongo/db/server_options.h"
 #include "mongo/db/service_context.h"
 #include "mongo/util/log.h"
 #include "mongo/util/scopeguard.h"
@@ -176,8 +177,10 @@ Status renameCollectionCommon(OperationContext* opCtx,
     // Ensure that collection name does not exceed maximum length.
     // Index names do not limit the maximum allowable length of the target namespace under
     // FCV 4.2 and above.
-    // TODO(SERVER-35824): Re-enable index namespace check under FCV 4.0.
-    const bool checkIndexNamespace = false;
+    const auto checkIndexNamespace =
+        serverGlobalParams.featureCompatibility.isVersionInitialized() &&
+        serverGlobalParams.featureCompatibility.getVersion() !=
+            ServerGlobalParams::FeatureCompatibility::Version::kFullyUpgradedTo42;
     std::string::size_type longestIndexNameLength =
         checkIndexNamespace ? sourceColl->getIndexCatalog()->getLongestIndexNameLength(opCtx) : 0;
     auto status = target.checkLengthForRename(longestIndexNameLength);