Although phytophagous insects can vary genetically in host use and exhibit long-range movements, the combined implications of these phenomena for pest management have received limited attention. To address this, we surveyed the genetic diversity of pea aphid Acyrthosiphon pisum using twelve microsatellite loci and assessed host association patterns and annual movement from a putative source region (Columbia River Basin) to the Palouse region of northern Idaho and western Washington, where the aphid is a pest of pea Pisum sativum. A total of 320 identified unique genotypes clustered into four genetic groups, with two host plant associations: alfalfa Medicago sativa (three genetic groups), and pea Pisum sativum and vetch Vicia villosa (one genetic group). All four genetic groups occurred in the Columbia River Basin and in migrant aphids collected in pan traps during spring colonization in the Palouse during 2 years of this study. Patterns of group arrival on the Palouse were spatially structured early in the season, consistent with differing migration patterns. Despite genetic diversity of migrants, a single genetic group became predominant in pea crops each year. Clonal laboratory colonies of pea aphids established from field-collected specimens and representing two predominant genetic groups exhibited reciprocal performance trade-offs, with alfalfa being a poor host for a pea-associated aphid genotype and vice versa. Synthesis and applications. Annual spring migrants of pea aphids in the pea production region of the Palouse are genetically diverse, with different host plant affinities consistent with origination from source populations in the Columbia River Basin. As the season progresses, a single genetic group adapted to pea becomes predominant in the crop. Management of pea aphid in the Palouse will be improved by monitoring the temporal and spatial variation of specific genetic groups of the aphid arriving as immigrants during each crop season, providing this information to producers and adjusting estimates of risk of crop damage accordingly. The principle could apply to other pest species with host-adapted populations that colonize crops on an annual basis.