diff --git a/containers/flatpak/test/test-browser-login-ssh.js b/containers/flatpak/test/test-browser-login-ssh.js
index 38e1129a97f4..32e5c57eb05a 100644
--- a/containers/flatpak/test/test-browser-login-ssh.js
+++ b/containers/flatpak/test/test-browser-login-ssh.js
@@ -12,9 +12,9 @@ async function test() {
         document.getElementById("server-field").value = "%HOST%";
         ph_mouse("#login-button", "click");
 
-        // unknown host key
-        await assert_conversation("authenticity of host");
-        document.getElementById("conversation-input").value = "yes";
+        // accept unknown host key
+        await ph_wait_present("#hostkey-message-1");
+        await ph_wait_in_text("#hostkey-message-1", "%HOST%");
         ph_mouse("#login-button", "click");
 
         await ph_wait_present("#conversation-prompt");
diff --git a/pkg/static/login.js b/pkg/static/login.js
index 65530cae3a31..200935ea9471 100644
--- a/pkg/static/login.js
+++ b/pkg/static/login.js
@@ -94,6 +94,15 @@ function debug(...args) {
         return document.getElementById(name);
     }
 
+    // strip off "user@", "*:port", and IPv6 brackets from login target (but keep two :: intact for IPv6)
+    function parseHostname(ssh_target) {
+        return ssh_target
+                .replace(/^.*@/, '')
+                .replace(/(?<!:):[0-9]+$/, '')
+                .replace(/^\[/, '')
+                .replace(/\]$/, '');
+    }
+
     // Hide an element (or set of elements) based on a boolean
     // true: element is hidden, false: element is shown
     function hideToggle(elements, toggle) {
@@ -596,10 +605,18 @@ function debug(...args) {
 
     // value of #server-field at the time of clicking "Login"
     let login_machine = null;
+    /* set by do_hostkey_verification() for a confirmed unknown host fingerprint;
+     * setup_localstorage() will then write the received full known_hosts entry to the known_hosts
+     * database for this host */
+    let login_data_host = null;
+    /* set if our known_host database has a non-matching host key, and we re-attempt the login
+     * with asking the user for confirmation */
+    let ssh_host_key_change_host = null;
 
     function call_login() {
         login_failure(null);
         login_machine = id("server-field").value;
+        login_data_host = null;
         const user = trim(id("login-user-input").value);
         if (user === "" && !environment.is_cockpit_client) {
             login_failure(_("User name cannot be empty"));
@@ -631,8 +648,27 @@ function debug(...args) {
             /* Keep information if login page was used */
             localStorage.setItem('standard-login', true);
 
+            let known_hosts = '';
+            if (login_machine) {
+                if (ssh_host_key_change_host == login_machine) {
+                    /* We came here because logging in ran into invalid-hostkey; so try the next
+                     * round without sending the key. do_hostkey_verification() will notice the
+                       change and show the correct dialog. */
+                    debug("call_login(): previous login attempt into", login_machine, "failed due to changed key");
+                } else {
+                    // If we have a known host key, send it to ssh
+                    const keys = get_hostkeys(login_machine);
+                    if (keys) {
+                        debug("call_login(): sending known_host key", keys, "for logging into", login_machine);
+                        known_hosts = keys;
+                    } else {
+                        debug("call_login(): no known_hosts entry for logging into", login_machine);
+                    }
+                }
+            }
+
             const headers = {
-                Authorization: "Basic " + window.btoa(utf8(user + ":" + password)),
+                Authorization: "Basic " + window.btoa(utf8(user + ":" + password + '\0' + known_hosts)),
                 "X-Superuser": superuser,
             };
             // allow unknown remote hosts with interactive logins with "Connect to:"
@@ -767,13 +803,13 @@ function debug(...args) {
     }
 
     function get_hostkeys(host) {
-        return get_known_hosts_db()[host];
+        return get_known_hosts_db()[parseHostname(host)];
     }
 
     function set_hostkeys(host, keys) {
         try {
             const db = get_known_hosts_db();
-            db[host] = keys;
+            db[parseHostname(host)] = keys;
             localStorage.setItem("known_hosts", JSON.stringify(db));
         } catch (ex) {
             console.warn("Can't write known_hosts database to localStorage", ex);
@@ -786,6 +822,7 @@ function debug(...args) {
         const key_type = key.split(" ")[1];
         const db_keys = get_hostkeys(key_host);
 
+        // code path for old C cockpit-ssh, which doesn't set a known_hosts file in advance (like beiboot)
         if (db_keys == key) {
             debug("do_hostkey_verification: received key matches known_hosts database, auto-accepting fingerprint", data.default);
             converse(data.id, data.default);
@@ -824,7 +861,16 @@ function debug(...args) {
         function call_converse() {
             id("login-button").removeEventListener("click", call_converse);
             login_failure(null, "hostkey");
-            set_hostkeys(key_host, key);
+            if (key.endsWith(" login-data")) {
+                // cockpit-beiboot sends only a placeholder, defer to login-data in setup_localstorage()
+                login_data_host = key_host;
+                debug("call_converse(): got placeholder host key (beiboot code path) for", login_data_host,
+                      ", deferring db update");
+            } else {
+                // cockpit-ssh already sends the actual key here
+                set_hostkeys(key_host, key);
+                debug("call_converse(): got real host key (cockpit-ssh code path) for", login_data_host);
+            }
             converse(data.id, data.default);
         }
 
@@ -950,6 +996,22 @@ function debug(...args) {
                 } else {
                     if (window.console)
                         console.log(xhr.statusText);
+                    /* did the user confirm a changed SSH host key? If so, update database */
+                    if (ssh_host_key_change_host) {
+                        try {
+                            const keys = JSON.parse(xhr.responseText)["known-hosts"];
+                            if (keys) {
+                                debug("send_login_request(): got updated known-hosts for changed host keys of", ssh_host_key_change_host, ":", keys);
+                                set_hostkeys(ssh_host_key_change_host, keys);
+                                ssh_host_key_change_host = null;
+                            } else {
+                                debug("send_login_request():", ssh_host_key_change_host, "changed key, but did not get an updated key from response");
+                            }
+                        } catch (ex) {
+                            console.error("Failed to parse response text as JSON:", xhr.responseText, ":", JSON.stringify(ex));
+                        }
+                    }
+
                     if (xhr.statusText.startsWith("captured-stderr:")) {
                         show_captured_stderr(decodeURIComponent(xhr.statusText.replace(/^captured-stderr:/, '')));
                     } else if (xhr.statusText.indexOf("authentication-not-supported") > -1) {
@@ -964,7 +1026,17 @@ function debug(...args) {
                     } else if (xhr.statusText.indexOf("unknown-host") > -1) {
                         host_failure(_("Refusing to connect. Host is unknown"));
                     } else if (xhr.statusText.indexOf("invalid-hostkey") > -1) {
-                        host_failure(_("Refusing to connect. Hostkey does not match"));
+                        /* ssh/ferny/beiboot immediately fail in this case, it's not a conversation;
+                         * ask the user for confirmation and try again */
+                        if (ssh_host_key_change_host === null) {
+                            debug("send_login_request(): invalid-hostkey, trying again to let the user confirm");
+                            ssh_host_key_change_host = login_machine;
+                            call_login();
+                        } else {
+                            // but only once, to avoid loops; this is also the code path for cockpit-ssh
+                            debug("send_login_request(): invalid-hostkey, and already retried, giving up");
+                            host_failure(_("Refusing to connect. Hostkey does not match"));
+                        }
                     } else if (is_conversation) {
                         login_failure(_("Authentication failed"));
                     } else {
@@ -1043,6 +1115,18 @@ function debug(...args) {
             localStorage.setItem(application + 'login-data', str);
             /* Backwards compatibility for packages that aren't application prefixed */
             localStorage.setItem('login-data', str);
+
+            /* When confirming a host key with cockpit-beiboot, login-data contains the known_hosts pubkey;
+             * update our database */
+            if (login_data_host) {
+                const hostkey = response["login-data"]["known-hosts"];
+                if (hostkey) {
+                    console.debug("setup_localstorage(): updating known_hosts database for deferred host key for", login_data_host, ":", hostkey);
+                    set_hostkeys(login_data_host, hostkey);
+                } else {
+                    console.error("login.js internal error: setup_localstorage() received a pending login-data host, but login-data does not contain known-hosts");
+                }
+            }
         }
 
         /* URL Root is set by cockpit ws and shouldn't be prefixed
diff --git a/src/cockpit/beiboot.py b/src/cockpit/beiboot.py
index 87cd9aa82189..8b577c2a881a 100644
--- a/src/cockpit/beiboot.py
+++ b/src/cockpit/beiboot.py
@@ -21,6 +21,7 @@
 import importlib.resources
 import logging
 import os
+import re
 import shlex
 import tempfile
 import time
@@ -167,14 +168,30 @@ async def do_askpass(self, messages: str, prompt: str, hint: str) -> Optional[st
             # Let's avoid all of that by just showing nothing.
             return None
 
+        # FIXME: is this a host key prompt? This should be handled more elegantly,
+        # see https://github.com/cockpit-project/cockpit/pull/19668
+        fp_match = re.search(r'\n(\w+) key fingerprint is ([^.]+)\.', prompt)
+        # let ssh resolve aliases, don't use our original "destination"
+        host_match = re.search(r"authenticity of host '([^ ]+) ", prompt)
+        args = {}
+        if fp_match and host_match:
+            # login.js do_hostkey_verification() expects host-key to be "hostname keytype key"
+            # we don't have access to the full key yet (that will be sent later as `login-data` challenge response),
+            # so just send a placeholder
+            args['host-key'] = f'{host_match.group(1)} {fp_match.group(1)} login-data'
+            # very oddly named, login.js do_hostkey_verification() expects the fingerprint here for user confirmation
+            args['default'] = fp_match.group(2)
+
         challenge_id = f'{os.getpid()}-{time.time()}'
         challenge_prefix = f'X-Conversation {challenge_id}'
         challenge = challenge_prefix + ' ' + base64.b64encode(prompt.encode()).decode()
         response = await self.router.request_authorization(challenge,
+                                                           timeout=None,
                                                            messages=messages,
                                                            prompt=prompt,
                                                            hint=hint,
-                                                           echo=False)
+                                                           echo=False,
+                                                           **args)
 
         if not response.startswith(challenge_prefix):
             raise CockpitProtocolError(
diff --git a/test/verify/check-client b/test/verify/check-client
index 704514c04ef9..aa8a81600b73 100755
--- a/test/verify/check-client
+++ b/test/verify/check-client
@@ -118,8 +118,9 @@ exec "$@"
         b.wait_not_visible("#recent-hosts-list")
         b.set_val("#server-field", "10.111.113.2")
         b.click("#login-button")
-        b.wait_in_text("#conversation-group", "authenticity of host '10.111.113.2")
-        b.set_val("#conversation-input", "yes")
+        # accept unknown host key
+        b.wait_in_text("#hostkey-message-1", "10.111.113.2")
+        b.wait_in_text("#hostkey-fingerprint", "SHA256:")
         b.click("#login-button")
         b.wait_text("#conversation-prompt", "admin@10.111.113.2's password: ")
         b.set_val("#conversation-input", "foobar")
diff --git a/test/verify/check-static-login b/test/verify/check-static-login
index dcd5000a5bbe..a5b6e9883e84 100755
--- a/test/verify/check-static-login
+++ b/test/verify/check-static-login
@@ -971,17 +971,17 @@ Command = /usr/bin/env python3 -m cockpit.beiboot
 """, append=True)
         m.start_cockpit()
 
-        def try_login(user, password, server=None):
+        def try_login(user, password, server=None, expect_hostkey=False):
             b.open("/")
             b.set_val('#login-user-input', user)
             b.set_val('#login-password-input', password)
             b.click("#show-other-login-options")
             b.set_val("#server-field", server or my_ip)
             b.click("#login-button")
-            # ack unknown host key; FIXME: this should be a proper authorize message, not a prompt
-            b.wait_in_text("#conversation-prompt", "authenticity of host")
-            b.set_val("#conversation-input", "yes")
-            b.click("#login-button")
+            if expect_hostkey:
+                b.wait_in_text("#hostkey-message-1", server or my_ip)
+                b.wait_in_text("#hostkey-fingerprint", "SHA256:")
+                b.click("#login-button")
 
         def check_no_processes():
             m.execute(f"while pgrep -af '[s]sh .* {my_ip}' >&2; do sleep 1; done")
@@ -996,13 +996,25 @@ Command = /usr/bin/env python3 -m cockpit.beiboot
             b.logout()
             check_no_processes()
 
+        def check_store_hostkey(expected: str) -> None:
+            db_hostkey = b.eval_js(f'JSON.parse(window.localStorage.getItem("known_hosts"))["{my_ip}"]')
+            if m.image.startswith('debian') or m.image.startswith('ubuntu'):
+                # these OSes encrypt host keys, so don't compare them
+                db_hostkey = ' '.join(db_hostkey.split()[1:])
+                expected = ' '.join(expected.split()[1:])
+            self.assertEqual(db_hostkey, expected)
+
         # successful login through SSH
-        try_login("admin", "foobar")
+        try_login("admin", "foobar", expect_hostkey=True)
         check_session()
+        # wrote full host key into session storage
+        # some OpenSSH versions add a comment here, filter that out
+        real_hostkey = m.execute(f"ssh-keyscan -t ssh-ed25519 {my_ip} | grep -v ^#")
+        check_store_hostkey(real_hostkey)
 
-        # wrong password
+        # host key is now known, but wrong password
         try_login("admin", "wrong")
-        b.wait_in_text("#login-error-message", "Authentication failed")
+        b.wait_text("#login-error-message", "Wrong user name or password")
         check_no_processes()
         # goes back to normal login form
         b.wait_visible('#login-user-input')
@@ -1013,7 +1025,7 @@ Command = /usr/bin/env python3 -m cockpit.beiboot
         check_session()
 
         # IPv6
-        try_login("admin", "foobar", server="::1")
+        try_login("admin", "foobar", server="::1", expect_hostkey=True)
         check_session(server="::1")
         try_login("admin", "foobar", server="[::1]:22")
         check_session(server="::1")
@@ -1031,6 +1043,35 @@ Command = /usr/bin/env python3 -m cockpit.beiboot
             m.execute("rm /etc/ssh/sshd_config.d/01-empty-password.conf")
             m.execute(self.restart_sshd)
 
+        # non-matching host key
+        bad_key = "172.27.0.15 ssh-ed25519 AAAAC3NzaC1lZDI1NTE5AAAAINKEIUL5s7ebg5Y6JdYNq4+mAaaaaaP1VRBDUiVdHT3R"
+        b.eval_js(f"""window.localStorage.setItem('known_hosts', '{{"{my_ip}": "{bad_key}"}}')""")
+
+        # first try with wrong credentials
+        try_login("admin", "wrong")
+        b.wait_text("#hostkey-title", f"{my_ip} key changed")
+        b.wait_in_text("#hostkey-fingerprint", "SHA256:")
+        b.click("#login-button.pf-m-danger")
+        b.wait_text("#login-error-message", "Authentication failed")
+        check_no_processes()
+        # new host key is accepted and updated in db
+        # confirmation replaces (not amends) known key
+        check_store_hostkey(real_hostkey)
+
+        # now with correct credentials, does not ask for host key any more
+        try_login("admin", "foobar")
+        check_session()
+        check_store_hostkey(real_hostkey)
+
+        # good credentials with bad key
+        b.eval_js(f"""window.localStorage.setItem('known_hosts', '{{"{my_ip}": "{bad_key}"}}')""")
+        try_login("admin", "foobar")
+        b.wait_text("#hostkey-title", f"{my_ip} key changed")
+        b.wait_in_text("#hostkey-fingerprint", "SHA256:")
+        b.click("#login-button.pf-m-danger")
+        check_session()
+        check_store_hostkey(real_hostkey)
+
 
 if __name__ == '__main__':
     testlib.test_main()