diff --git a/test/functional/feature_config_args.py b/test/functional/feature_config_args.py
index a1d22191a..e9924451d 100755
--- a/test/functional/feature_config_args.py
+++ b/test/functional/feature_config_args.py
@@ -29,8 +29,13 @@ class ConfArgsTest(BitcoinTestFramework):
 
         # Check that using non-existent datadir in conf file fails
         conf_file = os.path.join(default_data_dir, "bitcoin.conf")
-        with open(conf_file, 'a', encoding='utf8') as f:
+
+        # datadir needs to be set before [regtest] section
+        conf_file_contents = open(conf_file, encoding='utf8').read()
+        with open(conf_file, 'w', encoding='utf8') as f:
             f.write("datadir=" + new_data_dir + "\n")
+            f.write(conf_file_contents)
+
         self.nodes[0].assert_start_raises_init_error(['-conf=' + conf_file], 'Error reading configuration file: specified data directory "' + new_data_dir + '" does not exist.')
 
         # Create the directory and ensure the config file now works
diff --git a/test/functional/test_framework/util.py b/test/functional/test_framework/util.py
index f22322fbb..4ec3175cd 100644
--- a/test/functional/test_framework/util.py
+++ b/test/functional/test_framework/util.py
@@ -294,6 +294,7 @@ def initialize_datadir(dirname, n):
         os.makedirs(datadir)
     with open(os.path.join(datadir, "bitcoin.conf"), 'w', encoding='utf8') as f:
         f.write("regtest=1\n")
+        f.write("[regtest]\n")
         f.write("port=" + str(p2p_port(n)) + "\n")
         f.write("rpcport=" + str(rpc_port(n)) + "\n")
         f.write("server=1\n")