Understanding how climatic and environmental changes, as well as human activities, induce changes in the distribution and population size of avian species refines our ability to predict future impacts on threatened species. Using multilocus genetic data, we show that the population of a threatened New Zealand endemic open-habitat specialist, the Black-fronted Tern Chlidonias albostriatus – in contrast to forest specialists – expanded during the last glacial period. The population has decreased subsequently despite the availability of extensive open habitat after human arrival to New Zealand. We conclude that population changes for open habitat specialists such as Black-fronted Terns in pre-human New Zealand were habitat-dependent, similar to Northern Hemisphere cold-adapted species, whereas post-human settlement populations were constrained by predators independent of habitat availability, similar to other island endemic species.