Rabies is an ancient zoonotic disease caused by infection with the rabies virus (RABV). While the circulation of RABV in domestic dogs has been appreciated for centuries, the recognition of bat and wild carnivore reservoirs began in the early part of the 20th century. Bats are the ancestral reservoir of RABV and a remarkable diversity of species perpetuate distinct lineages of the virus, despite the fact that circulation in bats is geographically limited to the New World fauna. The circulation of RABV in domestic dogs likely represents a historic shift from a bat reservoir, although the timing and details of such an ancient event have been difficult to resolve from the virus genetic evidence. Since becoming established in the domestic dog population, RABV has undergone repeated host shifts to wild carnivores globally. These shifts have most frequently been to species within families of the Caniformia suborder of carnivores. The circulation of RABV in bats has been linked to host shifts to wild carnivore reservoirs in North and South America. It is clear that RABV has been incredibly successful at exploiting diverse chiropteran and carnivore hosts. With improved control of circulation in domestic dogs, surveillance is likely to yield additional discoveries regarding the diversity of wildlife reservoirs and vectors of RABV.