Geographic range expansion and population growth of vector-borne pathogens are regulated by the migration of their arthropod vectors. Recent climate and land-use changes have produced alterations in the geographic range and population size of blacklegged ticks (Ixodes scapularis) and the pathogens they vector, corresponding with the re-emergence of some of the most prevalent infectious diseases in North America. Relatively little empirical work has investigated the impact of range changes on the population dynamics and genetic structure of resulting populations during the precise time period in which they were colonized. This is due to the difficulties of collecting appropriate natural samples during the dynamic phase of migration and colonization. We systematically collected blacklegged ticks in New York State between 2004 and 2019, a time period directly coinciding with a rapid range expansion of ticks and the Lyme bacterium, Borrelia burgdorferi. These samples provide a unique opportunity to investigate the population dynamics and genetic structure of vectors and human pathogens as they expand into novel territory as well as the ability to characterize the degree to which vector and pathogen dynamics correspond with one another. We found evidence of genetic structure at broad geographic scale for both ticks and B. burgdorferi across New York, with genetic differentiation among populations driven by differences in the relative abundance, but not the composition, of haplotypes among sampled populations. We observed high levels of gene flow across the study region, with short-range migration events being significantly more common than long-range migration events. Despite high levels of gene flow, both tick and B. burgdorferi subpopulations remained genetically distinct from one another. Altogether, evidence suggests that tick and B. burgdorferi population dynamics are highly coordinated, despite each possessing unique ecological traits and spending considerable portions of their life-cycles independently of one another. Investigation of B. burgdorferi at finer scale revealed a wide range of interaction tendencies among genetically distinct lineages, necessitating future work to reconcile disparate patterns of B. burgdorferi population dynamics at fine and broad geographic scales.