Despite their recognized importance in the literature, the contribution of native-range species interactions to invasion success has been inadequately studied. Previous authors have suggested that biases in the sampling of propagules from the native range might influence invasion success, but most contemporary invasion hypotheses focus on the development of novel interactions or a release from native consumers and competitors. When ecotypic variation exists in native host-consumer associations, the specific pattern of sampling across ecotypes could determine invasion success, especially when the genetic diversity among exotic propagules is low. The South American cactus moth, Cactoblastis cactorum (Berg), is an oligophagous consumer whose larvae feed on prickly pear cacti (subfamily Opuntioideae). The moth was collected from a small geographic area along the Argentina-Uruguay border in 1925 and was introduced to multiple continents as a biological control species, which has subsequently invaded North America. Here we show that groups defined by genetic structure in this species’ native range are concordant with distinct patterns of host association and larval morphology. Furthermore, in Florida populations, morphological traits have diverged from those found in the native range, and patterns of host association suggest that strong biases in host preference also occur in invasive populations. The documented history of C. cactorum introductions confirms that multiple attempts were made to export the moth, but that only a single ecotype was exported successfully. Additional work will be necessary to determine whether the observed host biases in North America reflect a rapid adaptation to naive hosts or a conservation of traits related to specific aspects of the host-consumer association.