Tick-borne viruses are causative agents of several important human diseases. Tick-borne encephalitis virus (TBEV) is the most prominent representative considered medically to be the most important arbovirus (arthropod-borne virus) in Europe and northern Asia. Tick-borne virus transmission cycles are determined by the interactions between viruses, vectors, and their vertebrate hosts. Several mechanisms of tick-borne virus circulation in nature are currently considered to include transovarial transmission via the eggs from an infected female tick to its offspring, "viraemic" transmission between host and tick via feeding on a viraemic, infectious vertebrate hosts, and the virus transmission between co-feeding ticks, termed non-viraemic transmission (NVT). For NVT, the local skin site where ticks aggregately feed is an important focus of viral replication where migratory immune cells provide a vehicle for virus transmission from infected to uninfected co-feeding ticks. For TBEV at least, NVT is an important mechanism of virus maintenance in nature and offers explanations for some specific aspects of tick-borne virus ecology such as focal virus distribution and vector competency of particular tick species.