Information about similarities and differences in the demographic history of host and parasite populations is potentially useful for making inferences about a variety of evolutionary processes. However, it is difficult to observe the historical demographic properties of natural populations directly. Here, the extent of demographic similarity in a host and its parasite was examined indirectly by inferring long-term population history from patterns of genetic variation. Nucleotide sequence diversity in human and JC virus (JCV) DNA is consistent with a long-term demographic connection between the two species: both show evidence of large-scale population expansion. However, genetic data also suggest that the two species have different patterns of population substructuring. These similarities and differences have implications for adaptive evolution in JCV that are not evident when the two species are considered separately.