Conservation benefits from incorporating genomics to explore the impacts of population declines, inbreeding, loss of genetic variation and hybridization. Here we use the near-extinct Mariana Islands reedwarbler radiation to showcase how ancient DNA approaches can allow insights into the population dynamics of extinct species and threatened populations for which historical museum specimens or material with low DNA yield (e.g., scats, feathers) are the only sources for DNA. Despite their having paraphyletic mtDNA, nuclear SNPs support the distinctiveness of critically endangered Acrocephalus hiwae and the other three species in the radiation that went extinct between the 1960s and 1990s. Two extinct species, A. yamashinae and A. luscinius, were deeply divergent from each other and from a third less differentiated lineage containing A. hiwae and extinct A. nijoi. Both mtDNA and SNPs suggest that the two isolated populations of A. hiwae from Saipan and Alamagan Islands are sufficiently distinct to warrant subspecies recognition and separate conservation management. We detected no significant differences in genetic diversity or inbreeding between Saipan and Alamagan, nor strong signatures of geographic structuring within either island. However, the implications of possible signatures of inbreeding in both Saipan and Alamagan, and long-term population declines in A. hiwae that predate modern anthropogenic threats require further study with denser population sampling. Our study highlights the value conservation genomics studies of island radiations have as windows onto the possible future for the world’s biota as climate change and habitat destruction increasingly fragments their ranges and contributes to rapid declines in population abundances.