A virtual network interface controller (NIC) associated with a virtual machine in a cloud computing network is configured to support one or more network containers that encapsulate networking configuration data and policies that are applicable to a specific discrete computing workload to thereby enable the virtual machine to simultaneously belong to multiple virtual networks using the single NIC. The network containers supported by the NIC can be associated with a single tenant to enable additional flexibility such quickly switching between virtual networks and support pre-provisioning of additional computing resources with associated networking policies for rapid deployment. The network containers can also be respectively associated with different tenants so that the single NIC can support multi-tenant services on the same virtual machine.