Pteropids are large, highly mobile bats that are distributed widely across islands of the Pacific and Indian Oceans, southern Asia, and Australia. Dispersal behaviors and colonization patterns of pteropid species among oceanic islands are poorly known. In the southern Pacific, Pteropus samoensis and P. tonganus have partially overlapping ranges, existing in sympatry on the Samoan and Fijian archipelagos. These species exhibit differences in morphology and roosting behavior, with P. samoensis being smaller and tending to roost solitarily or in small groups. Here, we use genetic data to explore whether these species also exhibit differences with regard to patterns of population genetic structure within and between these archipelagos. Phylogenetic analyses of mitochondrial DNA are consistent with earlier morphological recognition of different subspecies of P. samoensis on the Samoan vs. Fijian archipelagos. Patterns of mtDNA haplotype sharing suggest that P. tonganus experiences restricted gene flow between, but not within archipelagos, while P. samoensis shows significant structuring both between and within archipelagos. Species-level differences in patterns of population structure among islands within archipelagos may be due to interspecific differences in morphology, roosting ecology, and/or feeding ecology that can be affected by human influences. Our results directly bear on the conservation of these species, suggesting that (1) populations of both species from the archipelagos of Samoa and Fiji should each be considered as separate conservation units, (2) P. samoensis are much less likely than P. tonganus to naturally supplement local populations through inter-island dispersal, and (3) P. tonganus may experience more severe population bottlenecks during and following cyclones resulting in lower mitochondrial genetic diversity than in P. samoensis.