The major lepidopteran insect pests of cotton and maize harbor intra-specific variation for behavior determining the selection of host plants for oviposition. Yet, the consequences of behavioral adaptation for fitness have neither been modeled nor monitored for Bt cotton and maize crops, the most widely grown transgenic herbivore-resistant plants. Here, we present a general two-locus heuristic model to examine potential outcomes of natural selection when pest populations initially have low frequencies of alleles for both physiological and behavioral adaptation to Bt crops. We demonstrate that certain ecological conditions allow for the evolution of behavioral choices favoring alternative oviposition hosts that limit the increase in resistance alleles, even when they are phenotypically dominant. These results have implications for current refuge policies, which should be adapted to promote the evolution of certain behavioral choices for alternative oviposition hosts in addition to dilution of physiological resistance alleles. Collection of data on oviposition host preference as a component of monitoring schemes will provide important insights into mechanisms underlying the durability of Bt-transgenic host-plant resistance.