Insect herbivores have been assumed to be more abundant in agricultural habitats than in native habitats; however, this hypothesis is rarely tested explicitly by comparing field populations of domesticated plants and their wild ancestors. This study examined the abundance of the sunflower moth, Homoeosoma electellum (Hulst), and its parasitism by natural enemies in agricultural and native sunflower habitats. Nutrient levels and plant population factors in the two habitat types were measured to identify factors associated with the patterns of herbivory and parasitism. Adult male and larval H. electellum were consistently more abundant in agricultural habitats. In contrast, parasitism of H. electellum was 6–10 times higher in native sunflower habitats than in agricultural habitats. Also, fewer parasitoid species were found in agricultural habitats, and parasitism by individual parasitoid species was reduced by 90%. Larval densities per flower head were higher on agricultural plants, but parasitoids failed to respond to the higher densities. The relationship between flower age and larval infestation differed between agricultural and wild flowers; larval age tracked agricultural flower age, but on wild flowers, larvae moved from older to younger flowers. Among the three nutrients sampled, only nitrogen was positively correlated with habitat differences. These results indicate that patterns of trophic interactions varied by habitat type and were related to plant phenotypic changes and environmental habitat factors such as crop domestication, nitrogen fertilization, and plant phenology.