Parasites in the genus Onchocerca infect humans, ruminants, camels, horses, suids, and canids, with effects ranging from relatively benign to debilitating. In North America, Onchocerca cervipedis is the sole species known to infect cervids, while at least 5 Onchocerca species infect Eurasian cervids. In this study, we report the discovery of a cervid-parasitizing Onchocerca only distantly related to O. cervipedis. To reconstruct the phylogenetic history of the genus Onchocerca, we used newly acquired DNA sequence from O. cervipedis (from moose in Northwest Territories, Canada) and from the newly discovered species (from white-tailed deer in upstate New York), as well as previously published sequences. Ancestral host reconstructions suggest that host switches have been common throughout the evolutionary history of Onchocerca, and that bovid- and cervid-parasitizing species have been particularly important sources of descendant species. North America cervids might therefore serve as a source for Onchocerca invasions into new hosts. Given the high density of deer populations, the potential for zoonotic infections may also exist. Our discovery of a new Onchocerca species with relatively limited sampling suggests that the diversity of Onchocerca associated with cervids in North America may be greater than previously thought, and surveys utilizing molecules and morphology are necessary.