diff --git a/pkg/networkmanager/dialogs-common.jsx b/pkg/networkmanager/dialogs-common.jsx
index 519ec18cb264..bad4c2d812eb 100644
--- a/pkg/networkmanager/dialogs-common.jsx
+++ b/pkg/networkmanager/dialogs-common.jsx
@@ -19,6 +19,7 @@
 
 import React, { useContext, useEffect, useState } from 'react';
 import cockpit from 'cockpit';
+import * as packagekit from 'packagekit.js';
 
 import { Button } from "@patternfly/react-core/dist/esm/components/Button/index.js";
 import { Checkbox } from "@patternfly/react-core/dist/esm/components/Checkbox/index.js";
@@ -35,11 +36,14 @@ import { IpSettingsDialog } from './ip-settings.jsx';
 import { TeamDialog, getGhostSettings as getTeamGhostSettings } from './team.jsx';
 import { TeamPortDialog } from './teamport.jsx';
 import { VlanDialog, getGhostSettings as getVlanGhostSettings } from './vlan.jsx';
+import { WireGuardDialog, getWireGuardGhostSettings } from './wireguard.jsx';
 import { MtuDialog } from './mtu.jsx';
 import { MacDialog } from './mac.jsx';
 import { ModalError } from 'cockpit-components-inline-notification.jsx';
 import { ModelContext } from './model-context.jsx';
 import { useDialogs } from "dialogs.jsx";
+import { install_dialog } from "cockpit-components-install-dialog.jsx";
+import { read_os_release } from "os-release.js";
 
 import {
     apply_group_member,
@@ -141,7 +145,7 @@ export const Name = ({ idPrefix, iface, setIface }) => {
     );
 };
 
-export const NetworkModal = ({ dialogError, help, idPrefix, title, onSubmit, children, isFormHorizontal, isCreateDialog }) => {
+export const NetworkModal = ({ dialogError, help, idPrefix, title, onSubmit, children, isFormHorizontal, isCreateDialog, submitDisabled = false }) => {
     const Dialogs = useDialogs();
 
     return (
@@ -152,7 +156,7 @@ export const NetworkModal = ({ dialogError, help, idPrefix, title, onSubmit, chi
             title={title}
             footer={
                 <>
-                    <Button variant='primary' id={idPrefix + "-save"} onClick={onSubmit}>
+                    <Button variant='primary' id={idPrefix + "-save"} onClick={onSubmit} isDisabled={submitDisabled}>
                         {isCreateDialog ? _("Add") : _("Save")}
                     </Button>
                     <Button variant='link' id={idPrefix + "-cancel"} onClick={Dialogs.close}>
@@ -198,10 +202,26 @@ export const NetworkAction = ({ buttonText, iface, connectionSettings, type }) =
         if (type == 'vlan') settings = getVlanGhostSettings();
         if (type == 'team') settings = getTeamGhostSettings({ newIfaceName });
         if (type == 'bridge') settings = getBridgeGhostSettings({ newIfaceName });
+        if (type == 'wg') settings = getWireGuardGhostSettings({ newIfaceName });
     }
 
     const properties = { connection: con, dev, settings };
 
+    async function resolveDeps(type) {
+        if (type === 'wg') {
+            try {
+                await cockpit.script("command -v wg");
+            } catch {
+                const packagekitExits = await packagekit.detect();
+                const os_release = await read_os_release();
+
+                // RHEL/CentOS 8 does not have wireguard-tools
+                if (packagekitExits && os_release.PLATFORM_ID !== "platform:el8")
+                    await install_dialog("wireguard-tools");
+            }
+        }
+    }
+
     function show() {
         let dlg = null;
         if (type == 'bond')
@@ -212,6 +232,8 @@ export const NetworkAction = ({ buttonText, iface, connectionSettings, type }) =
             dlg = <TeamDialog {...properties} />;
         else if (type == 'bridge')
             dlg = <BridgeDialog {...properties} />;
+        else if (type == 'wg')
+            dlg = <WireGuardDialog {...properties} />;
         else if (type == 'mtu')
             dlg = <MtuDialog {...properties} />;
         else if (type == 'mac')
@@ -224,8 +246,11 @@ export const NetworkAction = ({ buttonText, iface, connectionSettings, type }) =
             dlg = <IpSettingsDialog topic="ipv4" {...properties} />;
         else if (type == 'ipv6')
             dlg = <IpSettingsDialog topic="ipv6" {...properties} />;
+
         if (dlg)
-            Dialogs.show(dlg);
+            resolveDeps(type).then(() => {
+                Dialogs.show(dlg);
+            }).catch(console.error); // not-covered: OS error
     }
 
     return (
@@ -289,14 +314,18 @@ export const dialogSave = ({ model, dev, connection, members, membersInit, setti
                                      rollback_on_failure: type !== 'vlan' && membersChanged
                                  });
     } else {
-        with_checkpoint(
-            model,
-            modify,
-            {
-                fail_text: cockpit.format(_("Creating this $0 will break the connection to the server, and will make the administration UI unavailable."), type == 'vlan' ? 'VLAN' : type),
-                anyway_text: _("Create it"),
-                hack_does_add_or_remove: true,
-                rollback_on_failure: type != 'vlan',
-            });
+        try {
+            with_checkpoint(
+                model,
+                modify,
+                {
+                    fail_text: cockpit.format(_("Creating this $0 will break the connection to the server, and will make the administration UI unavailable."), type == 'vlan' ? 'VLAN' : type),
+                    anyway_text: _("Create it"),
+                    hack_does_add_or_remove: true,
+                    rollback_on_failure: type != 'vlan',
+                });
+        } catch (e) {
+            setDialogError(typeof e === 'string' ? e : e.message);
+        }
     }
 };
diff --git a/pkg/networkmanager/interfaces.js b/pkg/networkmanager/interfaces.js
index c3db37d76742..d91f34276970 100644
--- a/pkg/networkmanager/interfaces.js
+++ b/pkg/networkmanager/interfaces.js
@@ -585,6 +585,17 @@ export function NetworkManagerModel() {
             };
         }
 
+        if (settings.wireguard) {
+            result.wireguard = {
+                listen_port: get("wireguard", "listen-port", 0),
+                peers: get("wireguard", "peers", []).map(peer => ({
+                    publicKey: peer['public-key'].v,
+                    endpoint: peer.endpoint?.v, // enpoint of a peer is optional
+                    allowedIps: peer['allowed-ips'].v
+                })),
+            };
+        }
+
         return result;
     }
 
@@ -699,6 +710,33 @@ export function NetworkManagerModel() {
         } else
             delete result["802-3-ethernet"];
 
+        if (settings.wireguard) {
+            set("wireguard", "private-key", "s", settings.wireguard.private_key);
+            set("wireguard", "listen-port", "u", settings.wireguard.listen_port);
+            set("wireguard", "peers", "aa{sv}", settings.wireguard.peers.map(peer => {
+                return {
+                    "public-key": {
+                        t: "s",
+                        v: peer.publicKey
+                    },
+                    ...peer.endpoint
+                        ? {
+                            endpoint: {
+                                t: "s",
+                                v: peer.endpoint
+                            }
+                        }
+                        : {},
+                    "allowed-ips": {
+                        t: "as",
+                        v: peer.allowedIps
+                    }
+                };
+            }));
+        } else {
+            delete result.wireguard;
+        }
+
         return result;
     }
 
diff --git a/pkg/networkmanager/network-interface.jsx b/pkg/networkmanager/network-interface.jsx
index 2fbf2befaf2c..c1372343d516 100644
--- a/pkg/networkmanager/network-interface.jsx
+++ b/pkg/networkmanager/network-interface.jsx
@@ -560,6 +560,19 @@ export const NetworkInterfacePage = ({
             return renderSettingsRow(_("VLAN"), rows, configure);
         }
 
+        function renderWireGuardSettingsRow() {
+            const rows = [];
+            const options = settings.wireguard;
+
+            if (!options) {
+                return null;
+            }
+
+            const configure = <NetworkAction type="wg" iface={iface} connectionSettings={settings} />;
+
+            return renderSettingsRow(_("WireGuard"), rows, configure);
+        }
+
         return [
             render_group(),
             renderAutoconnectRow(),
@@ -571,7 +584,8 @@ export const NetworkInterfacePage = ({
             renderBridgePortSettingsRow(),
             renderBondSettingsRow(),
             renderTeamSettingsRow(),
-            renderTeamPortSettingsRow()
+            renderTeamPortSettingsRow(),
+            renderWireGuardSettingsRow(),
         ];
     }
 
@@ -681,7 +695,8 @@ export const NetworkInterfacePage = ({
     const isDeletable = (iface && !dev) || (dev && (dev.DeviceType == 'bond' ||
                                                     dev.DeviceType == 'team' ||
                                                     dev.DeviceType == 'vlan' ||
-                                                    dev.DeviceType == 'bridge'));
+                                                    dev.DeviceType == 'bridge' ||
+                                                    dev.DeviceType == 'wireguard'));
 
     const settingsRows = renderConnectionSettingsRows(iface.MainConnection, connectionSettings)
             .map((component, idx) => <React.Fragment key={idx}>{component}</React.Fragment>);
diff --git a/pkg/networkmanager/network-main.jsx b/pkg/networkmanager/network-main.jsx
index fe02734d4483..b623889d3afa 100644
--- a/pkg/networkmanager/network-main.jsx
+++ b/pkg/networkmanager/network-main.jsx
@@ -138,6 +138,7 @@ export const NetworkPage = ({ privileged, operationInProgress, usage_monitor, pl
 
     const actions = privileged && (
         <>
+            <NetworkAction buttonText={_("Add VPN")} type='wg' />
             <NetworkAction buttonText={_("Add bond")} type='bond' />
             <NetworkAction buttonText={_("Add team")} type='team' />
             <NetworkAction buttonText={_("Add bridge")} type='bridge' />
diff --git a/pkg/networkmanager/wireguard.jsx b/pkg/networkmanager/wireguard.jsx
new file mode 100644
index 000000000000..80c110589c7e
--- /dev/null
+++ b/pkg/networkmanager/wireguard.jsx
@@ -0,0 +1,353 @@
+/*
+ * This file is part of Cockpit.
+ *
+ * Copyright (C) 2023 Red Hat, Inc.
+ *
+ * Cockpit is free software; you can redistribute it and/or modify it
+ * under the terms of the GNU Lesser General Public License as published by
+ * the Free Software Foundation; either version 2.1 of the License, or
+ * (at your option) any later version.
+ *
+ * Cockpit is distributed in the hope that it will be useful, but
+ * WITHOUT ANY WARRANTY; without even the implied warranty of
+ * MERCHANTABILITY or FITNESS FOR A PARTICULAR PURPOSE. See the GNU
+ * Lesser General Public License for more details.
+ *
+ * You should have received a copy of the GNU Lesser General Public License
+ * along with Cockpit; If not, see <http://www.gnu.org/licenses/>.
+ */
+
+import React, { useContext, useEffect, useState } from 'react';
+import cockpit from 'cockpit';
+import { Button } from '@patternfly/react-core/dist/esm/components/Button/index.js';
+import { ClipboardCopy } from '@patternfly/react-core/dist/esm/components/ClipboardCopy/index.js';
+import { EmptyState, EmptyStateBody } from '@patternfly/react-core/dist/esm/components/EmptyState/index.js';
+import { FormGroup, FormFieldGroup, FormFieldGroupHeader, FormHelperText } from '@patternfly/react-core/dist/esm/components/Form/index.js';
+import { Flex, FlexItem } from "@patternfly/react-core/dist/esm/layouts/Flex/index.js";
+import { Grid } from '@patternfly/react-core/dist/esm/layouts/Grid/index.js';
+import { HelperText, HelperTextItem } from '@patternfly/react-core/dist/esm/components/HelperText/index';
+import { InputGroup } from '@patternfly/react-core/dist/esm/components/InputGroup/index.js';
+import { Popover } from '@patternfly/react-core/dist/esm/components/Popover/index.js';
+import { Radio } from '@patternfly/react-core/dist/esm/components/Radio/index.js';
+import { Text } from "@patternfly/react-core/dist/esm/components/Text/index.js";
+import { TextInput } from '@patternfly/react-core/dist/esm/components/TextInput/index.js';
+import { HelpIcon, TrashIcon } from '@patternfly/react-icons';
+
+import { Name, NetworkModal, dialogSave } from "./dialogs-common";
+import { ModelContext } from './model-context';
+import { useDialogs } from 'dialogs.jsx';
+
+import './wireguard.scss';
+
+const _ = cockpit.gettext;
+
+function addressesToString(addresses) {
+    return addresses.map(address => address[0] + "/" + address[1]).join(", ");
+}
+
+function stringToAddresses(str) {
+    return str.split(/[\s,]+/).map(strAddress => {
+        const parts = strAddress.split("/");
+        if (parts.length > 2) {
+            throw new Error(_("Addresses are not formatted correctly"));
+        }
+        const [ip, prefix] = parts;
+        const defaultPrefix = "32";
+        // Gateway usually conflicts with routing that NetworkManager configures for WireGuard interfaces
+        // So it should not be set in that case or more accurately set to 0 i.e. "0.0.0.0" in string format
+        const gateway = "0.0.0.0";
+        return [ip, prefix ?? defaultPrefix, gateway];
+    });
+}
+
+export function WireGuardDialog({ settings, connection, dev }) {
+    const Dialogs = useDialogs();
+    const idPrefix = "network-wireguard-settings";
+    const model = useContext(ModelContext);
+
+    const [iface, setIface] = useState(settings.connection.interface_name);
+    const [isPrivKeyGenerated, setIsPrivKeyGenerated] = useState(true);
+    const [generatedPrivateKey, setGeneratedPrivateKey] = useState("");
+    const [pastedPrivateKey, setPastedPrivatedKey] = useState("");
+    const [publicKey, setPublicKey] = useState("");
+    const [listenPort, setListenPort] = useState(settings.wireguard.listen_port);
+    const [addresses, setAddresses] = useState(addressesToString(settings.ipv4.addresses));
+    const [dialogError, setDialogError] = useState("");
+    const [peers, setPeers] = useState(settings.wireguard.peers.map(peer => ({ ...peer, allowedIps: peer.allowedIps.join(",") })));
+
+    // Additional check for `wg` after install_dialog for non-packagekit and el8 environments
+    useEffect(() => {
+        async function checkWireguardPackage() {
+            try {
+                await cockpit.script("command -v wg");
+            } catch (e) {
+                setDialogError(_("wireguard-tools package is not installed"));
+            }
+        }
+
+        checkWireguardPackage();
+    }, []);
+
+    useEffect(() => {
+        if (!connection) generatePrivateKey();
+    }, [connection]);
+
+    useEffect(() => {
+        async function getPrivateKey() {
+            const objpath = connection[" priv"].path;
+            const [result] = await model.client.call(objpath, "org.freedesktop.NetworkManager.Settings.Connection", "GetSecrets", ["wireguard"]);
+            setGeneratedPrivateKey(result.wireguard["private-key"].v);
+        }
+
+        if (connection?.[" priv"].path) {
+            getPrivateKey();
+        }
+    }, [model, connection]);
+
+    useEffect(() => {
+        const privateKey = isPrivKeyGenerated ? generatedPrivateKey : pastedPrivateKey;
+        if (privateKey === "") {
+            setPublicKey("");
+            return;
+        }
+
+        async function getPublicKey() {
+            try {
+                const key = await cockpit.spawn(["wg", "pubkey"], { err: 'message' }).input(privateKey.trim());
+                setPublicKey(key.trim());
+            } catch (e) {
+                console.error(e.message);
+                setPublicKey('');
+            }
+        }
+
+        getPublicKey();
+    }, [isPrivKeyGenerated, generatedPrivateKey, pastedPrivateKey]);
+
+    async function generatePrivateKey() {
+        try {
+            const key = await cockpit.spawn(["wg", "genkey"]);
+            setGeneratedPrivateKey(key.trim());
+        } catch (e) {
+            setDialogError(e.message);
+        }
+    }
+
+    function onSubmit() {
+        const private_key = isPrivKeyGenerated ? generatedPrivateKey : pastedPrivateKey;
+
+        // Validate Addresses before submit
+        // Also validate listenPort as PF TextInput[type=number] accepts normal text as well on firefox
+        // See - https://github.com/patternfly/patternfly-react/issues/9391
+        let addr, peersArr;
+        const listen_port = Number(listenPort);
+        try {
+            addr = stringToAddresses(addresses);
+
+            if (isNaN(listen_port)) {
+                throw new Error(_("Listen port must be a number"));
+            }
+
+            peersArr = peers.map((peer, index) => {
+                if (peer.endpoint !== '') {
+                    const parts = peer.endpoint.split(":");
+                    if (parts.length !== 2) {
+                        throw cockpit.format(_("Peer #$0 has invalid endpoint. It must be specified as host:port, e.g. 1.2.3.4:51820 or example.com:51820"), index + 1);
+                    }
+                    const [, port] = parts;
+                    if (port == '' || isNaN(Number(port))) {
+                        throw cockpit.format(_("Peer #$0 has invalid endpoint port. Port must be a number."), index + 1);
+                    }
+                }
+                return ({ ...peer, allowedIps: peer.allowedIps.split(',') });
+            });
+        } catch (e) {
+            setDialogError(typeof e === 'string' ? e : e.message);
+            return;
+        }
+
+        function createSettingsObj() {
+            return {
+                ...settings,
+                connection: {
+                    ...settings.connection,
+                    id: `con-${iface}`,
+                    interface_name: iface,
+                    type: 'wireguard'
+                },
+                wireguard: {
+                    private_key,
+                    listen_port,
+                    peers: peersArr,
+                },
+                ipv4: {
+                    addresses: addr,
+                    method: 'manual',
+                    dns: [],
+                    dns_search: []
+                }
+            };
+        }
+
+        dialogSave({
+            connection,
+            dev,
+            model,
+            settings: createSettingsObj(),
+            onClose: Dialogs.close,
+            setDialogError
+        });
+    }
+
+    return (
+        <NetworkModal
+            title={!connection ? _("Add WireGuard settings") : _("Edit WireGuard VPN")}
+            onSubmit={onSubmit}
+            dialogError={dialogError}
+            idPrefix={idPrefix}
+            submitDisabled={!iface || !addresses || !generatedPrivateKey}
+        >
+            <Name idPrefix={idPrefix} iface={iface} setIface={setIface} />
+            <FormGroup label={_("Private key")} fieldId={idPrefix + '-private-key-input'} isInline hasNoPaddingTop>
+                <Radio label={_("Generated")} name="private-key" id={idPrefix + '-generated-key'} defaultChecked onChange={() => { setIsPrivKeyGenerated(true) }} />
+                <Radio label={_("Paste existing key")} name="private-key" id={idPrefix + '-paste-key'} onChange={() => { setIsPrivKeyGenerated(false) }} />
+
+                {isPrivKeyGenerated
+                    ? <InputGroup className='pf-v5-u-pt-sm'>
+                        <Flex className='pf-v5-u-w-100' spaceItems={{ default: 'spaceItemsSm' }}>
+                            <FlexItem grow={{ default: 'grow' }}>
+                                <ClipboardCopy isReadOnly className='pf-v5-u-font-family-monospace pf-v5-u-w-100'>{generatedPrivateKey}</ClipboardCopy>
+                            </FlexItem>
+                            {connection && <FlexItem>
+                                <Button variant='secondary' onClick={generatePrivateKey}>{_("Regenerate")}</Button>
+                            </FlexItem>}
+                        </Flex>
+                    </InputGroup>
+                    : <InputGroup className='pf-v5-u-pt-sm'>
+                        <TextInput id={idPrefix + '-private-key-input'}
+                            className='pf-v5-u-font-family-monospace'
+                            value={pastedPrivateKey}
+                            onChange={(_, val) => setPastedPrivatedKey(val)}
+                            isDisabled={isPrivKeyGenerated}
+                        />
+                    </InputGroup>}
+            </FormGroup>
+            <FormGroup label={_("Public key")}>
+                {(isPrivKeyGenerated || publicKey)
+                    ? <ClipboardCopy isReadOnly className='pf-v5-u-font-family-monospace' id={idPrefix + '-public-key'}>{publicKey}</ClipboardCopy>
+                    : <Flex className='placeholder-text' alignItems={{ default: 'alignItemsCenter' }}><Text>{_("Public key will be generated when a valid private key is entered")}</Text></Flex>}
+            </FormGroup>
+            <FormGroup label={_("Listen port")} fieldId={idPrefix + '-listen-port-input'}>
+                <Flex gap={{ default: 'gapMd' }}>
+                    <TextInput id={idPrefix + '-listen-port-input'} className='network-number-field' value={listenPort} onChange={(_, val) => { setListenPort(val) }} />
+                    {!parseInt(listenPort) && <FormHelperText>
+                        <HelperText>
+                            <HelperTextItem>{_("Will be set to \"Automatic\"")}</HelperTextItem>
+                        </HelperText>
+                    </FormHelperText>}
+                </Flex>
+            </FormGroup>
+            <FormGroup label={_("IPv4 addresses")} fieldId={idPrefix + '-addresses-input'}>
+                <TextInput id={idPrefix + '-addresses-input'} value={addresses} onChange={(_, val) => { setAddresses(val) }} placeholder="Example, 10.0.0.1/24, 1.2.3.4/24" />
+                <FormHelperText>
+                    <HelperText>
+                        <HelperTextItem>{_("Multiple addresses can be specified using commas or spaces as delimiters.")}</HelperTextItem>
+                    </HelperText>
+                </FormHelperText>
+            </FormGroup>
+            <FormFieldGroup
+                header={
+                    <FormFieldGroupHeader
+                        titleText={{ text: _("Peers") }}
+                        actions={
+                            <>
+                                <Popover
+                                    bodyContent={
+                                        <p>{_("Peers are other machines that connect with this one. Public keys from other machines will be shared with each other.")}</p>
+                                    }
+                                    footerContent={
+                                        <p>{_("Endpoint acting as a \"server\" need to be specified as host:port, otherwise it can be left empty.")}</p>
+                                    }
+                                >
+                                    <Button variant='plain'><HelpIcon /></Button>
+                                </Popover>
+                                <Button
+                                    variant='secondary'
+                                    onClick={() => setPeers(peers => [...peers, { publicKey: '', endpoint: '', allowedIps: '' }])}
+                                >
+                                    {_("Add peer")}
+                                </Button>
+                            </>
+                        }
+                    />
+                }
+                className='dynamic-form-group'
+            >
+                {(peers.length !== 0)
+                    ? peers.map((peer, i) => (
+                        <Grid key={i} hasGutter id={idPrefix + '-peer-' + i}>
+                            <FormGroup className='pf-m-6-col-on-md' label={_("Public key")} fieldId={idPrefix + '-publickey-peer-' + i}>
+                                <TextInput
+                                    value={peer.publicKey}
+                                    onChange={(_, val) => {
+                                        setPeers(peers => peers.map((peer, index) => i === index ? { ...peer, publicKey: val } : peer));
+                                    }}
+                                    id={idPrefix + '-publickey-peer-' + i}
+                                />
+                            </FormGroup>
+                            <FormGroup className='pf-m-3-col-on-md' label={_("Endpoint")} fieldId={idPrefix + '-endpoint-peer-' + i}>
+                                <TextInput
+                                    value={peer.endpoint}
+                                    onChange={(_, val) => {
+                                        setPeers(peers => peers.map((peer, index) => i === index ? { ...peer, endpoint: val } : peer));
+                                    }}
+                                    id={idPrefix + '-endpoint-peer-' + i}
+                                />
+                            </FormGroup>
+                            <FormGroup className='pf-m-3-col-on-md' label={_("Allowed IPs")} fieldId={idPrefix + '-allowedips-peer-' + i}>
+                                <TextInput
+                                    value={peer.allowedIps}
+                                    onChange={(_, val) => {
+                                        setPeers(peers => peers.map((peer, index) => i === index ? { ...peer, allowedIps: val } : peer));
+                                    }}
+                                    id={idPrefix + '-allowedips-peer-' + i}
+                                />
+                            </FormGroup>
+                            <FormGroup className='pf-m-1-col-on-md remove-button-group'>
+                                <Button
+                                    variant='plain'
+                                    id={idPrefix + '-btn-close-peer-' + i}
+                                    onClick={() => {
+                                        setPeers(peers => peers.filter((_, index) => i !== index));
+                                    }}
+                                >
+                                    <TrashIcon />
+                                </Button>
+                            </FormGroup>
+                        </Grid>
+                    ))
+                    : <EmptyState>
+                        <EmptyStateBody>{_("No peers added.")}</EmptyStateBody>
+                    </EmptyState>
+                }
+            </FormFieldGroup>
+        </NetworkModal>
+    );
+}
+
+export function getWireGuardGhostSettings({ newIfaceName }) {
+    return {
+        connection: {
+            id: `con-${newIfaceName}`,
+            interface_name: newIfaceName
+        },
+        wireguard: {
+            listen_port: 0,
+            private_key: "",
+            peers: []
+        },
+        ipv4: {
+            addresses: []
+        }
+    };
+}
diff --git a/pkg/networkmanager/wireguard.scss b/pkg/networkmanager/wireguard.scss
new file mode 100644
index 000000000000..23f4fb37257d
--- /dev/null
+++ b/pkg/networkmanager/wireguard.scss
@@ -0,0 +1,38 @@
+@import "global-variables.scss";
+@import "@patternfly/patternfly/utilities/Text/text.scss";
+@import "@patternfly/patternfly/utilities/Spacing/spacing.scss";
+@import "@patternfly/patternfly/utilities/Sizing/sizing.scss";
+
+.placeholder-text {
+  color: var(--pf-v5-global--Color--200);
+  block-size: 2.25rem;
+}
+
+.dynamic-form-group {
+  .pf-v5-c-empty-state {
+    padding: 0;
+  }
+
+  .pf-v5-c-form__field-group-body {
+    .pf-v5-c-form__group {
+      display: block;
+    }
+
+    .remove-button-group {
+      // Move 'Remove' button the the end of the row
+      grid-column: -1;
+      // Move 'Remove' button to the bottom of the line so as to align with the other form fields
+      display: flex;
+      align-items: flex-end;
+    }
+  }
+
+  // We use FormFieldGroup PF component for the nested look and for ability to add buttons to the header
+  // However we want to save space and not add indent to the left so we need to override it
+  .pf-v5-c-form__field-group-body {
+    // Stretch content fully
+    --pf-v5-c-form__field-group-body--GridColumn: 1 / -1;
+    // Reduce padding at the top
+    --pf-v5-c-form__field-group-body--PaddingTop: var(--pf-v5-global--spacer--xs);
+  }
+}
diff --git a/test/run b/test/run
index a2e6839ada19..8beee5eaa8a7 100755
--- a/test/run
+++ b/test/run
@@ -12,7 +12,7 @@ PREPARE_OPTS=""
 RUN_OPTS=""
 ALL_TESTS="$(test/common/run-tests --test-dir test/verify -l)"
 
-RE_NETWORKING='Networking|Bonding|TestBridge|Firewall|Team|IPA|AD'
+RE_NETWORKING='Networking|Bonding|TestBridge|WireGuard|Firewall|Team|IPA|AD'
 RE_STORAGE='Storage'
 RE_EXPENSIVE='HostSwitching|MultiMachine|Updates|Superuser|Kdump|Pages'
 
diff --git a/test/verify/check-networkmanager-wireguard b/test/verify/check-networkmanager-wireguard
new file mode 100755
index 000000000000..ba6c6481bc90
--- /dev/null
+++ b/test/verify/check-networkmanager-wireguard
@@ -0,0 +1,194 @@
+#!/usr/bin/python3 -cimport os, sys; os.execv(os.path.dirname(sys.argv[1]) + "/../common/pywrap", sys.argv)
+
+import subprocess
+import sys
+
+import netlib
+import packagelib
+import testlib
+
+
+class TestWireGuard(packagelib.PackageCase, netlib.NetworkCase):
+    provision = {
+        "machine1": {"address": "192.168.100.11/24", "restrict": False},
+        "machine2": {"address": "192.168.100.12/24", "restrict": False},
+    }
+
+    def testVPN(self):
+        m1 = self.machines["machine1"]
+        m2 = self.machines["machine2"]
+        b = self.browser
+
+        self.login_and_go("/network")
+
+        # Peer 1 (client)
+        m1_port = 51820
+        m1_ip4 = "10.0.0.1"
+        m1_ip6 = "2001::1"
+        b.click("button:contains('Add VPN')")
+        b.wait_visible("#network-wireguard-settings-dialog")
+        iface_name = b.val("#network-wireguard-settings-interface-name-input")
+        b.wait_visible("button:contains('Save'):disabled")
+        if m1.image in ["rhel4edge", "centos-8-stream"] or m1.image.startswith("rhel-8"):
+            b.wait_visible(".pf-v5-c-alert:contains('wireguard-tools package is not installed')")
+            b.click("button:contains('Cancel')")
+            b.wait_not_present("#network-ip-settings-dialog")
+            b.wait_visible("#networking")
+            b.wait_not_present(f"#networking-interfaces th:contains('{iface_name}')")
+            # Skip the rest of the tests for images without wireguard-tools
+            # As without it private/public key, connection over IPv4/IPv6 etc can't be tested
+            return
+
+        # Peer 2 (server)
+        m2_port = 51820
+        m2_ip4 = "10.0.0.2"
+        m2_ip6 = "2001::2"
+        if not m2.ostree_image:
+            m2.execute(f"firewall-cmd --add-port={m2_port}/udp")
+        m2.execute("wg genkey > private")
+        m2_pubkey = m2.execute("wg pubkey < private").strip()
+        m2.execute("ip link add dev wg0 type wireguard")
+        m2.execute(f"ip addr add {m2_ip4}/24 dev wg0")
+        m2.execute("wg set wg0 private-key ./private")
+        m2.execute(f"wg set wg0 listen-port {m2_port}")
+        m2.execute("ip link set wg0 up")
+
+        # Validate each field, enter the right value, and then proceed to the next field
+        #
+        # check private-key
+        b.click("#network-wireguard-settings-paste-key")
+        b.set_input_text("#network-wireguard-settings-private-key-input", "incorrect key")
+        b.set_input_text("#network-wireguard-settings-addresses-input", m1_ip4)
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('key must be 32 bytes base64 encoded')")
+        b.click("#network-wireguard-settings-generated-key")
+
+        # check public-key
+        b.wait_not_val("#network-wireguard-settings-public-key input", "")
+        m1_pubkey = b.val("#network-wireguard-settings-public-key input")
+
+        # check listen-port
+        b.set_input_text("#network-wireguard-settings-listen-port-input", "66000")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('out of range')")
+        b.set_input_text("#network-wireguard-settings-listen-port-input", "sometext")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Listen port must be a number')")
+        b.set_input_text("#network-wireguard-settings-listen-port-input", str(m1_port))
+
+        # check ip addresses
+        b.set_input_text("#network-wireguard-settings-addresses-input", "10.0.0.1/24/56")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Addresses are not formatted correctly')")
+        b.set_input_text("#network-wireguard-settings-addresses-input", "10.0.0")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Invalid address 10.0.0')")
+        b.set_input_text("#network-wireguard-settings-addresses-input", "ten.one")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Invalid address ten.one')")
+        b.set_input_text("#network-wireguard-settings-addresses-input", "10 1")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Invalid address 10')")
+        b.set_input_text("#network-wireguard-settings-addresses-input", "1.2.3.4/")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Invalid prefix or netmask')")
+        b.set_input_text("#network-wireguard-settings-addresses-input", "1.2.3.4  ,  5.6.7.8  1.2.3.4.5")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Invalid address 1.2.3.4.5')")
+        b.set_input_text("#network-wireguard-settings-addresses-input", f"{m1_ip4}/24 1.2.3.4")
+
+        # peer
+        b.click("button:contains('Add peer')")
+        b.wait_visible("#network-wireguard-settings-peer-0")
+        b.set_input_text("#network-wireguard-settings-publickey-peer-0", m2_pubkey)
+        b.set_input_text("#network-wireguard-settings-endpoint-peer-0", f"192.168.100.12")
+        b.set_input_text("#network-wireguard-settings-allowedips-peer-0", m2_ip4)
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Peer #1 has invalid endpoint. It must be specified as host:port, e.g. 1.2.3.4:51820 or example.com:51820')")
+        b.set_input_text("#network-wireguard-settings-endpoint-peer-0", f"192.168.100.12:somestring")
+        b.click("button:contains('Save')")
+        b.wait_visible(".pf-v5-c-alert:contains('Peer #1 has invalid endpoint port. Port must be a number.')")
+        b.click("button:contains('Add peer')")
+        b.wait_visible("#network-wireguard-settings-peer-1")
+        b.set_input_text("#network-wireguard-settings-publickey-peer-1", m2_pubkey)
+        b.set_input_text("#network-wireguard-settings-endpoint-peer-1", f"192.168.100.12:{m2_port}")
+        b.set_input_text("#network-wireguard-settings-allowedips-peer-1", m2_ip4)
+        b.click("button#network-wireguard-settings-btn-close-peer-0")
+        b.wait_not_present("#network-wireguard-settings-peer-1")
+        b.click("button:contains('Save')")
+        b.wait_not_present("#network-wireguard-settings-dialog")
+        b.wait_in_text(f"#networking-interfaces th:contains('{iface_name}') + td", f"1.2.3.4/32, {m1_ip4}/24")
+
+        # endpoint and port is not necessary for a peer if that peer estalishes the connectio first (i.e. the client)
+        m2.execute(f"wg set wg0 peer {m1_pubkey} allowed-ips {m1_ip4}/32")
+
+        # check connection over ipv4
+        try:
+            m1.execute(f"ping -c 5 {m2_ip4}")
+        except (subprocess.CalledProcessError, testlib.Error):
+            print("-------- status on m1 ----------", file=sys.stderr)
+            m1.execute("set -x; ip a >&2; ip route >&2; nmcli c >&2; wg >&2")
+            print("-------- status on m2 ----------", file=sys.stderr)
+            m2.execute("set -x; ip a >&2; ip route >&2; nmcli c >&2; wg >&2")
+            raise
+
+        # check connection over ipv6
+        m2.execute(f"ip addr add {m2_ip6}/64 dev wg0")
+        m2.execute(f"wg set wg0 peer {m1_pubkey} allowed-ips {m1_ip4}/32,{m1_ip6}")
+
+        b.click(f"#networking-interfaces button:contains('{iface_name}')")
+        b.click("#networking-edit-wg")
+        b.wait_visible("#network-wireguard-settings-dialog")
+        b.set_input_text("#network-wireguard-settings-allowedips-peer-0", f"{m2_ip4}/32,{m2_ip6}")
+        b.click("button:contains('Save')")
+        b.wait_not_present("#network-wireguard-settings-dialog")
+
+        m1.execute("until wg show wg0 | grep -q 'allowed ips.*2001::2/128'; do sleep 1; done")
+
+        b.click("#networking-edit-ipv6")
+        b.wait_visible("#network-ip-settings-dialog")
+        b.select_from_dropdown("#network-ip-settings-select-method", "manual")
+        b.set_input_text("#network-ip-settings-address-0", m1_ip6)
+        b.set_input_text("#network-ip-settings-netmask-0", "64")
+        b.set_input_text("#network-ip-settings-gateway-0", "::")
+        b.click("button:contains('Save')")
+        b.wait_not_present("#network-ip-settings-dialog")
+        self.wait_for_iface_setting("IPv6", "Address 2001:0:0:0:0:0:0:1/64")
+
+        m1.execute(f"until ip a show dev {iface_name} | grep -q 'inet6 {m1_ip6}/64 scope global'; do sleep 0.3; done", timeout=10)
+
+        try:
+            m1.execute(f"ping -6 -c 5 {m2_ip6}")
+        except (subprocess.CalledProcessError, testlib.Error):
+            print("-------- status on m1 ----------", file=sys.stderr)
+            m1.execute("set -x; ip a >&2; ip -6 route >&2; nmcli c >&2; wg >&2")
+            print("-------- status on m2 ----------", file=sys.stderr)
+            m2.execute("set -x; ip a >&2; ip -6 route >&2; nmcli c >&2; wg >&2")
+            raise
+
+        # install wireguard-tools from the install dialog
+        if not m1.ostree_image:
+            b.go("/network")
+            m1.execute("pkcon remove -y wireguard-tools")
+            self.createPackage("wireguard-tools", "1", "1")
+            self.enableRepo()
+            # HACK: Packagekit on Arch Linux does not deal well with detecting new repositories
+            if m1.image == "arch":
+                m1.execute("systemctl restart packagekit")
+                m1.execute("pkcon refresh force")
+            b.click("button:contains('Add VPN')")
+            b.wait_visible("#dialog button:contains('Install'):enabled")
+            b.click("#dialog button:contains('Install')")
+            b.wait_not_present("#dialog")
+            b.wait_visible("#network-wireguard-settings-dialog")
+            b.wait_visible(".pf-v5-c-alert")
+            b.click("button:contains('Cancel')")
+
+        # lastly delete the interface
+        b.click(f"#networking-interfaces button:contains('{iface_name}')")
+        b.click("#network-interface-delete")
+        b.wait_not_present(f"#networking-interfaces th:contains('{iface_name}')")
+
+
+if __name__ == "__main__":
+    testlib.test_main()