Since first human settlement c. 400 years ago, the Mascarene islands have undergone some of the highest rates of ecosystem transformation and species extinction recorded worldwide. One surviving species, the Mascarene Swiftlet Aerodramus francicus native to the islands of Mauritius and Réunion, is typical among Aerodramus swiftlets in presenting a paucity of distinguishable morphological characters, as well as being particularly vulnerable to anthropogenic activities. In this study, a primary objective was generating genetic data for each island population, allowing genetic divergence between them to be assessed for the first time, employing informative methods regarding the taxonomic status. We find that the two island populations are 0.8% divergent and reciprocally monophyletic in the mitochondrial ND2 gene, with nuclear data (β-fibrinogen intron 7) being largely congruent but showing incomplete lineage sorting and low resolution. Results of barcode gap and coalescent species delimitation analyses are consistent with a comparison of the genetic divergence uncovered within Mascarene Aerodramus with that among other long-established Aerodramus species. The findings of all three approaches are consistent with the two island populations representing two separate species. However, because of lack of resolution in the nuclear locus, we conservatively retain a single species pending future data. To assess the conservation status, we conducted the first quantitative assessment of population size and distribution through extensive nest counts on the islands of Mauritius and Réunion, and by considering the threats to swiftlets on each island. The survey produced estimates of 10,100–10,700 individuals for Mauritius, and 39,600–53,500 individuals for Réunion. Considering the population size data, inferred distributions, and numerous conservation concerns, an updated conservation status to Threatened (Endangered): B2 b(i,ii,iii,iv,v) c(i,ii,iii,iv) is warranted according to IUCN guidelines. Improving protection of the breeding habitat of the Mascarene Swiftlet is crucial to prevent this endemic species from being added to the Mascarene's staggering extinction toll.