Adaptive evolution of pest insects in response to the introduction of resistant cultivars is well documented and commonly results in virulent (i.e., capable of feeding upon resistant cultivars) insect populations being labeled as distinct biotypes. Phenotypically defined, biotypes frequently remain evolutionarily indistinct, resulting in ineffective application of virulence control measures and shorter durability of resistant cultivars. Here, we utilize an evolutionary framework to discern the genetic relationship between biotypes of the soybean aphid (Aphis glycines, Matsumura). The soybean aphid is invasive in North America and is among the most destructive pests of commercial soybean on the continent. Attempts to breed host-plant-resistant soybean have been hampered by the emergence of virulent aphid biotypes that are unaffected by the plant's resistance mechanism(s). Comparative population genetic analysis of virulent and avirulent (i.e., unable to feed on resistant cultivars) biotypes found populations to be genetically indistinguishable across biotype and geographic distance, with high rates of interpopulation immigration and admixture. The lack of genetic distinction between biotypes coupled with elevated genotypic diversity within all populations suggested virulence has a nongenetic-based or includes a gene complex that is widely distributed throughout soybean aphid populations, which undergo regular dispersal and unimpeded sexual recombination.