Adaptation to human-induced environmental change has the potential to profoundly influence the genomic architecture of affected species. This is particularly true in agricultural ecosystems, where anthropogenic selection pressure is strong. Heliothis virescens primarily feeds on cotton in its larval stages and US populations have been declining since the widespread planting of transgenic cotton, which endogenously expresses proteins derived from Bacillus thuringiensis (Bt). No physiological adaptation to Bt toxin has been found in the field, so adaptation in this altered environment could involve: 1) shifts in host plant selection mechanisms to avoid cotton, 2) changes in detoxification mechanisms required for cotton-feeding versus feeding on other hosts, or 3) loss of resistance to previously used management practices including insecticides. Here we begin to address whether such changes occurred in H. virescens populations between 1997-2012, as Bt cotton cultivation spread through the agricultural landscape. For our study, we produced an H. virescens genome assembly and used this in concert with a ddRAD-seq enabled genome scan to identify loci with significant allele frequency changes over the 15 year period. Genetic changes at a previously described H. virescens insecticide target of selection were detectable in our genome scan, and increased our confidence in this methodology. Additional loci were also detected as being under selection, and we quantified the selection strength required to elicit observed allele frequency changes at each locus. Potential contributions of genes near loci under selection to adaptive phenotypes in the H. virescens cotton system are discussed.