diff --git a/test/functional/interface_bitcoin_cli.py b/test/functional/interface_bitcoin_cli.py
index f626ee51761..fbe753a65fa 100755
--- a/test/functional/interface_bitcoin_cli.py
+++ b/test/functional/interface_bitcoin_cli.py
@@ -6,6 +6,7 @@
 
 from decimal import Decimal
 import re
+import subprocess
 
 from test_framework.blocktools import COINBASE_MATURITY
 from test_framework.netutil import test_ipv6_local
@@ -434,6 +435,16 @@ class TestBitcoinCli(BitcoinTestFramework):
         self.log.info("Test that only one of -addrinfo, -generate, -getinfo, -netinfo may be specified at a time")
         assert_raises_process_error(1, "Only one of -getinfo, -netinfo may be specified", self.nodes[0].cli('-getinfo', '-netinfo').send_cli)
 
+        if not self.is_ipc_compiled():
+            # This tests behavior when ENABLE_IPC is off. When it is on,
+            # behavior is checked by the interface_ipc_cli.py test.
+            self.log.info("Test bitcoin-cli -ipcconnect triggers error if not built with IPC support")
+            args = [self.binary_paths.bitcoincli, "-ipcconnect=unix", "-getinfo"]
+            result = subprocess.run(args, stdout=subprocess.PIPE, stderr=subprocess.STDOUT, text=True)
+            assert_equal(result.stdout, "error: bitcoin-cli was not built with IPC support\n")
+            assert_equal(result.stderr, None)
+            assert_equal(result.returncode, 1)
+
 
 if __name__ == '__main__':
     TestBitcoinCli(__file__).main()
diff --git a/test/functional/interface_ipc_cli.py b/test/functional/interface_ipc_cli.py
new file mode 100755
index 00000000000..92ccc879fba
--- /dev/null
+++ b/test/functional/interface_ipc_cli.py
@@ -0,0 +1,68 @@
+#!/usr/bin/env python3
+# Copyright (c) 2025 The Bitcoin Core developers
+# Distributed under the MIT software license, see the accompanying
+# file COPYING or http://www.opensource.org/licenses/mit-license.php.
+"""Test IPC with bitcoin-cli"""
+
+from test_framework.test_framework import BitcoinTestFramework
+from test_framework.util import (
+    assert_equal,
+    rpc_port
+)
+
+import subprocess
+
+class TestBitcoinIpcCli(BitcoinTestFramework):
+    def set_test_params(self):
+        self.setup_clean_chain = True
+        self.num_nodes = 1
+
+    def skip_test_if_missing_module(self):
+        self.skip_if_no_ipc()
+
+    def setup_nodes(self):
+        self.extra_init = [{"ipcbind": True}]
+        super().setup_nodes()
+
+    def test_cli(self, args, error=None):
+        # Intentionally set wrong RPC password so only IPC not HTTP connections work
+        args = [self.binary_paths.bitcoincli, f"-datadir={self.nodes[0].datadir_path}", "-rpcpassword=wrong"] + args + ["echo", "foo"]
+        result = subprocess.run(args, stdout=subprocess.PIPE, stderr=subprocess.STDOUT, text=True)
+        if error is None:
+            assert_equal(result.stdout, '[\n  "foo"\n]\n')
+        else:
+            assert_equal(result.stdout, error)
+        assert_equal(result.stderr, None)
+        assert_equal(result.returncode, 0 if error is None else 1)
+
+    def run_test(self):
+        node = self.nodes[0]
+        if node.ipc_tmp_dir:
+            self.log.info("Skipping a few checks because temporary directory path is too long")
+
+        http_auth_error = "error: Authorization failed: Incorrect rpcuser or rpcpassword\n"
+        http_connect_error = f"error: timeout on transient error: Could not connect to the server 127.0.0.1:{rpc_port(node.index)}\n\nMake sure the bitcoind server is running and that you are connecting to the correct RPC port.\nUse \"bitcoin-cli -help\" for more info.\n"
+        ipc_connect_error = "error: timeout on transient error: Connection refused\n\nProbably bitcoin-node is not running or not listening on a unix socket. Can be started with:\n\n    bitcoin-node -chain=regtest -ipcbind=unix\n"
+        ipc_http_conflict = "error: -rpcconnect and -ipcconnect options cannot both be enabled\n"
+
+        for started in (True, False):
+            auto_error = None if started else http_connect_error
+            http_error = http_auth_error if started else http_connect_error
+            ipc_error = None if started else ipc_connect_error
+
+            if not node.ipc_tmp_dir:
+                self.test_cli([], auto_error)
+                self.test_cli(["-rpcconnect=127.0.0.1"], http_error)
+                self.test_cli(["-ipcconnect=auto"], auto_error)
+                self.test_cli(["-ipcconnect=auto", "-rpcconnect=127.0.0.1"], http_error)
+                self.test_cli(["-ipcconnect=unix"], ipc_error)
+
+            self.test_cli([f"-ipcconnect=unix:{node.ipc_socket_path}"], ipc_error)
+            self.test_cli(["-noipcconnect"], http_error)
+            self.test_cli(["-ipcconnect=unix", "-rpcconnect=127.0.0.1"], ipc_http_conflict)
+
+            self.stop_node(0)
+
+
+if __name__ == '__main__':
+    TestBitcoinIpcCli(__file__).main()
diff --git a/test/functional/test_runner.py b/test/functional/test_runner.py
index a4052f91024..8d80b5a78ff 100755
--- a/test/functional/test_runner.py
+++ b/test/functional/test_runner.py
@@ -379,6 +379,7 @@ BASE_SCRIPTS = [
     'tool_rpcauth.py',
     'p2p_handshake.py',
     'p2p_handshake.py --v2transport',
+    'interface_ipc_cli.py',
     'feature_dirsymlinks.py',
     'feature_help.py',
     'feature_framework_startup_failures.py',