diff --git a/pyinfra/connectors/sshuserclient/client.py b/pyinfra/connectors/sshuserclient/client.py
index 362c99cb9..4dd88a055 100644
--- a/pyinfra/connectors/sshuserclient/client.py
+++ b/pyinfra/connectors/sshuserclient/client.py
@@ -14,6 +14,7 @@
     SSHException,
 )
 from paramiko.agent import AgentRequestHandler
+from paramiko.hostkeys import HostKeyEntry
 
 from pyinfra import logger
 from pyinfra.api.util import memoize
@@ -31,6 +32,28 @@ def missing_host_key(self, client, hostname, key):
         )
 
 
+def append_hostkey(client, hostname, key):
+    """Append hostname to the clients host_keys_file"""
+
+    with HOST_KEYS_LOCK:
+        # The paramiko client saves host keys incorrectly whereas the host keys object does
+        # this correctly, so use that with the client filename variable.
+        # See: https://github.com/paramiko/paramiko/pull/1989
+        host_key_entry = HostKeyEntry([hostname], key)
+        if host_key_entry is None:
+            raise SSHException(
+                "Append Hostkey: Failed to parse host {0}, could not append to hostfile".format(
+                    hostname
+                ),
+            )
+        with open(client._host_keys_filename, "a") as host_keys_file:
+            hk_entry = host_key_entry.to_line()
+            if hk_entry is None:
+                raise SSHException(f"Append Hostkey: Failed to append hostkey ({host_key_entry})")
+
+            host_keys_file.write(hk_entry)
+
+
 class AcceptNewPolicy(MissingHostKeyPolicy):
     def missing_host_key(self, client, hostname, key):
         logger.warning(
@@ -40,13 +63,8 @@ def missing_host_key(self, client, hostname, key):
             ),
         )
 
-        with HOST_KEYS_LOCK:
-            host_keys = client.get_host_keys()
-            host_keys.add(hostname, key.get_name(), key)
-            # The paramiko client saves host keys incorrectly whereas the host keys object does
-            # this correctly, so use that with the client filename variable.
-            # See: https://github.com/paramiko/paramiko/pull/1989
-            host_keys.save(client._host_keys_filename)
+        append_hostkey(client, hostname, key)
+        logger.warning("Added host key for {0} to known_hosts".format(hostname))
 
 
 class AskPolicy(MissingHostKeyPolicy):
@@ -60,13 +78,7 @@ def missing_host_key(self, client, hostname, key):
             raise SSHException(
                 "AskPolicy: No host key for {0} found in known_hosts".format(hostname),
             )
-        with HOST_KEYS_LOCK:
-            host_keys = client.get_host_keys()
-            host_keys.add(hostname, key.get_name(), key)
-            # The paramiko client saves host keys incorrectly whereas the host keys object does
-            # this correctly, so use that with the client filename variable.
-            # See: https://github.com/paramiko/paramiko/pull/1989
-            host_keys.save(client._host_keys_filename)
+        append_hostkey(client, hostname, key)
         logger.warning("Added host key for {0} to known_hosts".format(hostname))
         return
 
diff --git a/tests/test_connectors/test_sshuserclient.py b/tests/test_connectors/test_sshuserclient.py
index 3c3c17450..28f1468a3 100644
--- a/tests/test_connectors/test_sshuserclient.py
+++ b/tests/test_connectors/test_sshuserclient.py
@@ -1,7 +1,8 @@
+from base64 import b64decode
 from unittest import TestCase
 from unittest.mock import mock_open, patch
 
-from paramiko import ProxyCommand
+from paramiko import PKey, ProxyCommand, SSHException
 
 from pyinfra.connectors.sshuserclient import SSHClient
 from pyinfra.connectors.sshuserclient.client import AskPolicy, get_ssh_config
@@ -41,6 +42,30 @@
 Include other_file
 """
 
+# To ensure that we don't remove things from users hostfiles
+# we should test that all modifications only append to the
+# hostfile, and don't delete any data or comments.
+EXAMPLE_KEY_1 = (
+    "AAAAB3NzaC1yc2EAAAADAQABAAABgQCj7ndNxQowgcQnjshcLrqPEiiphnt+"
+    "VTTvDP6mHBL9j1aNUkY4Ue1gvwnGLVlOhGeYrnZaMgRK6+PKCUXaDbC7qtbW8gIkhL7aGCsOr/"
+    "C56SJMy/BCZfxd1nWzAOxSDPgVsmerOBYfNqltV9/hWCqBywINIR+5dIg6JTJ72pcEpEjcYgXk"
+    "E2YEFXV1JHnsKgbLWNlhScqb2UmyRkQyytRLtL+38TGxkxCflmO+5Z8CSSNY7GidjMIZ7Q4zMj"
+    "A2n1nGrlTDkzwDCsw+wqFPGQA179cnfGWOWRVruj16z6XyvxvjJwbz0wQZ75XK5tKSb7FNyeIE"
+    "s4TT4jk+S4dhPeAUC5y+bDYirYgM4GC7uEnztnZyaVWQ7B381AK4Qdrwt51ZqExKbQpTUNn+Ej"
+    "qoTwvqNj4kqx5QUCI0ThS/YkOxJCXmPUWZbhjpCg56i+2aB6CmK2JGhn57K5mj0MNdBXA4/Wnw"
+    "H6XoPWJzK5Nyu2zB3nAZp+S5hpQs+p1vN1/wsjk="
+)
+
+KNOWN_HOSTS_EXAMPLE_DATA = f"""
+# this is an important comment
+
+# another comment after the newline
+
+@cert-authority example-domain.lan ssh-rsa {EXAMPLE_KEY_1}
+
+192.168.1.222 ssh-rsa {EXAMPLE_KEY_1}
+"""
+
 
 class TestSSHUserConfigMissing(TestCase):
     def setUp(self):
@@ -199,3 +224,45 @@ def test_test_paramiko_connect_kwargs(self, fake_paramiko_connect):
             port=22,
             test="kwarg",
         )
+
+    def test_missing_hostkey(self):
+        client = SSHClient()
+        policy = AskPolicy()
+        example_hostname = "new_host"
+        example_keytype = "ecdsa-sha2-nistp256"
+        example_key = (
+            "AAAAE2VjZHNhLXNoYTItbmlzdHAyNT"
+            "YAAAAIbmlzdHAyNTYAAABBBHNp1NM"
+            "ZjxPBuuKwIPfkVJqWaH3oUtW137kIW"
+            "P4PlCyACt8zVIIimFhIpwRUidcf7jw"
+            "VWPAJvfBjEPqewDApnZQ="
+        )
+
+        key = PKey.from_type_string(
+            example_keytype,
+            b64decode(example_key),
+        )
+
+        # Check if AskPolicy respects not importing and properly raises SSHException
+        with self.subTest("Check user 'no'"):
+            with patch("builtins.input", return_value="n"):
+                self.assertRaises(
+                    SSHException, lambda: policy.missing_host_key(client, example_hostname, key)
+                )
+
+        # Check if AskPolicy properly appends to hostfile
+        with self.subTest("Check user 'yes'"):
+            mock_data = mock_open(read_data=KNOWN_HOSTS_EXAMPLE_DATA)
+            # Read mock hostfile
+            with patch("pyinfra.connectors.sshuserclient.client.open", mock_data):
+                with patch("paramiko.hostkeys.open", mock_data):
+                    with patch("builtins.input", return_value="y"):
+                        policy.missing_host_key(client, "new_host", key)
+
+            # Assert that we appended correctly to the file
+            write_call_args = mock_data.return_value.write.call_args
+            # Ensure we only wrote once and then closed the handle.
+            assert len(write_call_args) == 2
+            # Ensure we wrote the correct content
+            correct_output = f"{example_hostname} {example_keytype} {example_key}\n"
+            assert write_call_args[0][0] == correct_output