Intraspecific variation in ecologically important traits is a cornerstone of Darwin’s theory of evolution by natural selection. The evolution and maintenance of this variation depends on genetic architecture, which in turn determines responses to natural selection. Some models suggest that traits with complex architectures are less likely to respond to selection than those with simple architectures, yet rapid divergence has been observed in such traits. The simultaneous evolutionary lability and genetic complexity of host plant use in the Lepidopteran subfamily Heliothinae suggest that architecture may not constrain ecological adaptation in this group. Here we investigate the response of Chloridea virescens, a generalist that feeds on diverse plant species, to selection for performance on a novel host, Physalis angulata (Solanaceae). P. angulata is the preferred host of Chloridea subflexa, a narrow specialist on the genus Physalis. In previous experiments, we found that the performance of C. subflexa on P. angulata depends on many loci of small effect distributed throughout the genome, but whether the same architecture would be involved in the generalist’s adoption of P. angulata was unknown. Here we report a rapid response to selection in C. virescens for performance on P. angulata, and establish that the genetic architecture of intraspecific variation is quite similar to that of the interspecific differences in terms of the number, distribution, and effect sizes of the QTL involved. We discuss the impact of genetic architecture on the ability of Heliothine moths to respond to varying ecological selection pressures.