Small, mobile insects are notoriously challenging to track across landscapes and manage in agricultural fields. However, genetic differentiation among insect populations and host-plants acquired through host-associated differentiation could be exploited to infer movement within crop systems and damage potential. Although many insects exhibit host-associated differentiation, management strategies for insect vectors of plant pathogens assume a homogenous population. Nevertheless, phenotypic changes derived from host-associated differentiation could manifest in altered behavior or physiology affecting the likelihood of vector-pathogen-plant interactions, or the subsequent efficiency of pathogen transmission. We used SNPs to assess genotypic structure and host-associated differentiation in the cowpea aphid, Aphis craccivora Koch (Hemiptera: Aphididae). To do so, we sampled A. craccivora across the Midwestern U.S. from two host-plants, alfalfa (Medicago sativa) and black locust (Robinia pseudoacacia) — putative source populations for winged migrants. Simultaneously, we sampled winged A. craccivora landing in pumpkin fields where they transmit viruses. Structure analyses supported host-associated differentiation by identifying two major genotypic groups: an alfalfa group containing a single multilocus genotype, and a locust group containing all others. Winged locust-group aphids landed at a much greater magnitude within focal fields during year 2 than year 1, while those in the alfalfa-group remained fairly consistent. Spatial autocorrelation analyses indicated locust-group aphid movementwas characterized by small-scale dispersal during year 2, likely originating from populations within 10 km. We also detected strong temporal differences in colonization from the two host-plants. Early in the summer, most winged aphids (79.4%) derived from the locust group, whereas late in the summer more (58.3%) were from the alfalfa group. Because early crop growth stages are more susceptible to damage from aphid-vectored viruses, these data implicate locust as the more important source and illustrate how host-associated differentiation can be used to track dispersal and inform management of heterogeneous pest populations.