Recurrent specialization on similar host plants offers a unique opportunity to unravel the evolutionary and genetic mechanisms underlying dietary shifts. Recent studies have focused on ecological races belonging to the same species, but it is hard in many cases to untangle the role of adaptive introgression versus distinct mutations in facilitating recurrent evolution. We discovered on the island of Mayotte a population of the generalist fly Drosophila yakuba that is strictly associated with noni (Morinda citrifolia). This case strongly resembles Drosophila sechellia, a genetically isolated insular relative of D. yakuba whose intensely studied specialization on toxic noni fruits has always been considered a unique event in insect evolution. Experiments revealed that unlike mainland D. yakuba strains, Mayotte flies showed strong olfactory attraction and significant toxin tolerance to noni. Island females strongly discriminated against mainland males, suggesting that dietary adaptation has been accompanied by partial reproductive isolation. Population genomic analysis indicated a recent colonization (∼29 kya), at a time when year-round noni fruits may have presented a predictable resource on the small island, with ongoing migration after colonization. This relatively recent time scale allowed us to search for putatively adaptive loci based on genetic variation. Strong signals of genetic differentiation were found for several detoxification genes, including a major toxin tolerance locus in D. sechellia. Our results suggest that recurrent evolution on a toxic resource can involve similar historical events and common genetic bases, and they establish an important genetic system for the study of early stages of ecological specialization and speciation.host plant adaptation | ecological genomics | parallel evolution | island speciation | Drosophila yakuba E ver since Darwin's (1) description of finch diversity on the Galapagos archipelago, dietary specialization has been considered a major drive of speciation by means of natural selection. Adaptation to similar diets have led to the parallel evolution of beak morphology in some species inhabiting different islands, but genome analyses revealed that this was most likely due to the adaptive introgression of the underlying loci between species (2). In herbivorous insects, host plant specialization also plays a major role in diversification (3), and spectacular examples of convergent evolution both in plant resistant toxins and insect toxin resistances spanning hundred million of years of divergence have been observed. For example, several unrelated flowering plants produce cardenolides that block activity of the ion gradient regulating enzyme (Na + +K + )ATPase in insects, but identical cardenolideresistant amino acid substitutions in this enzyme have independently arisen in beetles, butterflies, flies, and aphids specializing on such plants (4). Recent genomic studies have focused on parallel dietary shifts in early-diverging ecological races, pointing to a substantial d...