Multi-tenant network stack techniques are described. In an implementation, a host instantiates an instance of virtual machine that is configured to serve networks service to multiple tenants and corresponding virtual networks. To do so, a framing layer of the virtual machine may be configured to obtain configuration data indicative of topology for a multi-tenant virtual networking environment from a virtual switch of a host device. The framing layer uses the configuration data to construct routing compartments and interfaces as abstractions of each virtual network in accordance with the topology. The routing compartments are isolated from each other and provide a mechanism for applications to process network input/output (I/O) in the context of a specific tenant or virtual network. The single virtual machine is able to provide services and applications to serve multiple tenants that are independent of the underlying virtualization technology.