Surveys of patterns of genetic variation in natural sympatric and allopatric populations of recently diverged species are necessary to understand the processes driving intra and interspecific diversification. The South American moths Cactoblastis cactorum, Cactoblastis doddi and Cactoblastis bucyrus are specialized in the use of cacti as host plants. These species have different distribution ranges and differ in patterns of host plant use. However, there are areas in which their ranges overlap, as in northwestern Argentina, where they are largely sympatric. Using a combination of genome-wide SNPs and mitochondrial data we investigated the phylogeographic patterns of these cactophilic moths and searched for footprints of hybridization. Additionally, we evaluated a moth population feeding on Cleistocactus baumannii, a plant never reported as a host for the genus. We identified three well delimited species and detected signs of historical gene flow. Our survey also revealed intraspecific geographic structure in both C. doddi and C. cactorum and showed that the moth population feeding on C. baumannii may be considered as conspecific to C. bucyrus. Overall, our results indicated historical events of genetic interchange occurred in Cactoblastis cactophagous moths, but host plants likely played an important role during divergence limiting gene flow across species.