Resource partitioning may facilitate the coexistence of sympatric species with similar ecological requirements. Here, we study a colony of unusual echolocating birds called swiftlets, which nest underground on an island off the coast of Singapore. The colony comprises two congeneric swiftlet species, black-nest swiftlets (Aerodramus maximus) and edible-nest swiftlets (A. fuciphagus), nesting at high densities and in close proximity. Bioacoustic recordings and monitoring of nesting biology at the site across multiple seasons revealed significant differences in echolocation calls as well as survival rates between the species, with the larger black-nest swiftlet nesting at locations with the highest fledging rates. We also observe an additional off-season breeding peak by the smaller species, the edible-nest swiftlet. Unexpectedly, off-season egg hatching rates were significantly higher compared to rates during the shared breeding season (mean difference = 14%). Our study on the breeding biology of these echolocating cave-dwelling birds provides an example of spatial and temporal strategies that animals employ to partition resources within a confined habitat.