Ustilago maydis virus H1 (Umv-H1) is a mycovirus that infects Ustilago maydis, a fungal pathogen of maize. As Zea mays was domesticated, it carried with it many associated symbionts, such that the subsequent range expansion and cultivation of maize should have affected maize symbionts' evolutionary history dramatically. Because transmission of Umv-H1 takes place only through cytoplasmic fusion during mating of U. maydis individuals, the population dynamics of U. maydis and maize are expected to affect the population structure of the viral symbiont strongly. Here, the impact of changes in the evolutionary history of U. maydis on that of Umv-H1 was investigated. The high mutation rate of this virus allows inferences to be made about the evolution and divergence of Umv-H1 lineages as a result of the recent changes in U. maydis geographical and genetic structure. The phylogeographical history and genetic structure of Umv-H1 populations in the USA and Mexico were determined by using analyses of viral nucleotide sequence variation. Infection and recombination frequencies, genetic diversity and rates of neutral evolution were also assessed, to make inferences regarding evolutionary processes underlying the population genetic structure of ancestral and descendent populations. The results suggest that Mexico represents the ancestral population of Umv-H1, from which the virus has been carried with U. maydis populations into the USA. Thus, the population dynamics of one symbiont represent a major evolutionary force on the co-evolutionary dynamics of symbiotic partners.