Described herein are systems, methods, and software to manage the updates for a container runtime. In one example, a host identifies a request to update a container runtime from a first version to a second version for a container executing in a virtual machine. The host further initiates execution of a second container in a second virtual machine with the second version of the container runtime, wherein the second container uses the same root filesystem as the first container. The host also updates any required networking configurations to direct communications to the second container over the first container and stops execution of the first container.