Changes in climate and land-use are influencing the spatial distributions and population structure of species throughout the world. Among those species predicted to be affected by changes in climate and land-use are the hosts and vectors of many zoonotic pathogens, including the hosts and vectors of the Lyme borreliosis pathogen, Borrelia burgdorferi. In this study, we investigate the population structure of B. burgdorferi at the interface of two expanding vector populations using a population genetic and phylogeographic approach. We then examine the influence of recombination between major B. burgdorferi lineages on the population structure of B. burgdorferi within and between geographic regions. We found that B. burgdorferi lineages were heterogeneously distributed between the Northeast and Southeast United States, suggesting that gene flow between geographic regions is limited for some lineages while other lineages showed evidence of long distance dispersal. We identified at least two clonal B. burgdorferi lineages present in both competent vector species found in southern Virginia, suggesting that vector species is not a barrier to dispersal between regions. Population genetic and phylogeographic analyses of B. burgdorferi reveal a complicated pattern of population structure within and between geographic regions. Population genomic analyses show recombination between lineages despite evidence of strong linkage disequilibrium and a lack of genetic variation within B. burgdorferi lineages, suggesting a small effective population size.