diff --git a/changelogs/fragments/9743-incus_connection-nonroot-user.yml b/changelogs/fragments/9743-incus_connection-nonroot-user.yml
new file mode 100644
index 0000000000..f1a7aa9b5f
--- /dev/null
+++ b/changelogs/fragments/9743-incus_connection-nonroot-user.yml
@@ -0,0 +1,2 @@
+minor_changes:
+  - incus connection plugin - adds ``remote_user`` and ``incus_become_method`` parameters for allowing a non-root user to connect to an Incus instance (https://github.com/ansible-collections/community.general/pull/9743).
diff --git a/plugins/connection/incus.py b/plugins/connection/incus.py
index 326e91ec38..842ad8f924 100644
--- a/plugins/connection/incus.py
+++ b/plugins/connection/incus.py
@@ -32,6 +32,15 @@ options:
     vars:
       - name: ansible_executable
       - name: ansible_incus_executable
+  incus_become_method:
+    description:
+      - Become command used to switch to a non-root user.
+      - Is only used when O(remote_user) is not V(root).
+    type: str
+    default: /bin/su
+    vars:
+      - name: incus_become_method
+    version_added: 10.4.0
   remote:
     description:
       - The name of the Incus remote to use (per C(incus remote list)).
@@ -40,6 +49,22 @@ options:
     default: local
     vars:
       - name: ansible_incus_remote
+  remote_user:
+    description:
+      - User to login/authenticate as.
+      - Can be set from the CLI via the C(--user) or C(-u) options.
+    type: string
+    default: root
+    vars:
+      - name: ansible_user
+    env:
+      - name: ANSIBLE_REMOTE_USER
+    ini:
+      - section: defaults
+        key: remote_user
+    keyword:
+      - name: remote_user
+    version_added: 10.4.0
   project:
     description:
       - The name of the Incus project to use (per C(incus project list)).
@@ -64,7 +89,6 @@ class Connection(ConnectionBase):
 
     transport = "incus"
     has_pipelining = True
-    default_user = 'root'
 
     def __init__(self, play_context, new_stdin, *args, **kwargs):
         super(Connection, self).__init__(play_context, new_stdin, *args, **kwargs)
@@ -79,10 +103,34 @@ class Connection(ConnectionBase):
         super(Connection, self)._connect()
 
         if not self._connected:
-            self._display.vvv("ESTABLISH Incus CONNECTION FOR USER: root",
+            self._display.vvv(f"ESTABLISH Incus CONNECTION FOR USER: {self.get_option('remote_user')}",
                               host=self._instance())
             self._connected = True
 
+    def _build_command(self, cmd) -> str:
+        """build the command to execute on the incus host"""
+
+        exec_cmd = [
+            self._incus_cmd,
+            "--project", self.get_option("project"),
+            "exec",
+            f"{self.get_option('remote')}:{self._instance()}",
+            "--"]
+
+        if self.get_option("remote_user") != "root":
+            self._display.vvv(
+                f"INFO: Running as non-root user: {self.get_option('remote_user')}, \
+                trying to run 'incus exec' with become method: {self.get_option('incus_become_method')}",
+                host=self._instance(),
+            )
+            exec_cmd.extend(
+                [self.get_option("incus_become_method"), self.get_option("remote_user"), "-c"]
+            )
+
+        exec_cmd.extend([self.get_option("executable"), "-c", cmd])
+
+        return exec_cmd
+
     def _instance(self):
         # Return only the leading part of the FQDN as the instance name
         # as Incus instance names cannot be a FQDN.
@@ -95,13 +143,8 @@ class Connection(ConnectionBase):
         self._display.vvv(f"EXEC {cmd}",
                           host=self._instance())
 
-        local_cmd = [
-            self._incus_cmd,
-            "--project", self.get_option("project"),
-            "exec",
-            f"{self.get_option('remote')}:{self._instance()}",
-            "--",
-            self._play_context.executable, "-c", cmd]
+        local_cmd = self._build_command(cmd)
+        self._display.vvvvv(f"EXEC {local_cmd}", host=self._instance())
 
         local_cmd = [to_bytes(i, errors='surrogate_or_strict') for i in local_cmd]
         in_data = to_bytes(in_data, errors='surrogate_or_strict', nonstring='passthru')
@@ -120,6 +163,25 @@ class Connection(ConnectionBase):
 
         return process.returncode, stdout, stderr
 
+    def _get_remote_uid_gid(self) -> tuple[int, int]:
+        """Get the user and group ID of 'remote_user' from the instance."""
+
+        rc, uid_out, err = self.exec_command("/bin/id -u")
+        if rc != 0:
+            raise AnsibleError(
+                f"Failed to get remote uid for user {self.get_option('remote_user')}: {err}"
+            )
+        uid = uid_out.strip()
+
+        rc, gid_out, err = self.exec_command("/bin/id -g")
+        if rc != 0:
+            raise AnsibleError(
+                f"Failed to get remote gid for user {self.get_option('remote_user')}: {err}"
+            )
+        gid = gid_out.strip()
+
+        return int(uid), int(gid)
+
     def put_file(self, in_path, out_path):
         """ put a file from local to Incus """
         super(Connection, self).put_file(in_path, out_path)
@@ -130,12 +192,35 @@ class Connection(ConnectionBase):
         if not os.path.isfile(to_bytes(in_path, errors='surrogate_or_strict')):
             raise AnsibleFileNotFound(f"input path is not a file: {in_path}")
 
-        local_cmd = [
-            self._incus_cmd,
-            "--project", self.get_option("project"),
-            "file", "push", "--quiet",
-            in_path,
-            f"{self.get_option('remote')}:{self._instance()}/{out_path}"]
+        if self.get_option("remote_user") != "root":
+            uid, gid = self._get_remote_uid_gid()
+            local_cmd = [
+                self._incus_cmd,
+                "--project",
+                self.get_option("project"),
+                "file",
+                "push",
+                "--uid",
+                str(uid),
+                "--gid",
+                str(gid),
+                "--quiet",
+                in_path,
+                f"{self.get_option('remote')}:{self._instance()}/{out_path}",
+            ]
+        else:
+            local_cmd = [
+                self._incus_cmd,
+                "--project",
+                self.get_option("project"),
+                "file",
+                "push",
+                "--quiet",
+                in_path,
+                f"{self.get_option('remote')}:{self._instance()}/{out_path}",
+            ]
+
+        self._display.vvvvv(f"PUT {local_cmd}", host=self._instance())
 
         local_cmd = [to_bytes(i, errors='surrogate_or_strict') for i in local_cmd]