Winter ticks (Dermacentor albipictus) on elk (Cervus elaphus canadensis) have recently increased in numbers in the Yukon, Canada, potentially posing risks to other indigenous host species in the region. To evaluate the regional source of winter ticks in the Yukon, we sequenced one nuclear (ITS-2) and two mitochondrial (16SrRNA and COI) genes, and genotyped 14 microsatellite loci from 483 winter tick specimens collected across North America. We analyzed genetic variation across the geographic and host ranges of this tick species with the use of variance partitioning, Bayesian clustering, and standard population genetic analyses. Based on our results, winter ticks on elk in the Yukon could have originated either by translocation from central Alberta or by northward range expansion of more geographically proximate populations in northern Alberta and British Columbia. Although there was some genetic structuring of winter ticks on different hosts in the same region, we found little evidence of host specificity in winter ticks from five ungulate host species, suggesting that the winter ticks on elk in the Yukon could potentially become established on other locally available host species such as moose (Alces alces).