We examined population genetics and kinship in 10 colony-based groupings of Afro-Malagasy Otomops from three species: near-threatened O. martiensseni from eastern South Africa (6 colonies); newly-described O. harrisoni from northeast Africa (3 colonies); and O. madagascariensis from Madagascar (1 colony, least concern). Our aim was to compare genetic structure based on 6 nuclear microsatellites with that based on mitochondrial cytochrome b and D-loop sequence data, at both species and colony level. Further, we aimed to shed light on social structure in Otomops by analysing gene flow, migration, relatedness and kinship among and within colonies. Three major lineages were identified in analyses of nuclear and mitochondrial datasets, separated by significant (p < 0.01) pairwise FST values, consistent with O. martiensseni, O. harrisoni and O. madagascariensis. Pairwise FST and mean relatedness values between colonies from the same species lineage were lower than those between lineages. 70% of individuals sampled were part of either parent/offspring, full-sibling or half-sibling relationships within geographically-based species level lineages, whereas no kinship was observed across lineages. Two parent/offspring dyads were identified within colonies belonging to the O. martiensseni lineage and one within the O. harrisoni lineage, whereas no parent/offspring dyads were established between colonies. Full-sibling and half-sibling pairs were observed both within and between colonies within their respective lineages. However, most kinship within lineages took the form of half-sibling relationships, reinforcing the suggestion that Otomops engages in extra-colony mating. Our results suggest that individuals do not exhibit strict colony faithfulness, and that gene flow is maintained through extra-colony mating. We find little evidence to support the presence of a social system based on either female or male philopatry in Afro-Malagasy Otomops.