Honeybees are present on all islands of the South Western Indian Ocean (SWIO), including Madagascar and three surrounding archipelagos (the Comoros, Seychelles and Mascarenes). If Apis mellifera unicolor is indubitably an African subspecies endemic to Madagascar, its relationship with insular honey bee populations from this hotspot of biodiversity is misunderstood and its ecological role in natural ecosystems still poorly documented. In such a context, the evolutionary history of the species in the SWIO is pertinent to explore. The aims were to (i) characterize the genetic origins and diversity of the insular populations (ii) test whether morphological and genetic divergences among populations correlate and (iii) investigate the ecological role through the study of biotic interactions with the native ¿ora. In collaboration with regional partners, a dataset of more than 4 000 colonies sampled in Mada-gascar and the 9 surrounding islands were considered for genetic, morphometric and genomic analyses. Mitochondrial screening indicated that insular populations belong to one private African sub-group, but also revealed recent human importation of European subspecies in the Mascarene Islands (Mauritius, Rodrigues, La R´eunion). Nuclear DNA analyses highlighted signi¿cant genetic di¿erentiations among insular populations from this African sub-group, suggesting ancient colonization events. When con-fronted, the patterns of genetic and morphological diversi¿cation observed were highly congruent both at the inter- and intra-archipelago scales. In Reunion, whole genome sequencing of individuals (n=36) showed admixture between African and European lineages, with however a higher level of A. mellifera unicolor mitotype. Results provide insights into the long- term consequences of introducing exotic specimens on the nuclear genome and indirectly on the morphology of locally adapted populations. Ecological surveys conducted in natural forest ecosystems from Madagascar and La Reuni