Arctic birds and mammals are physiologically adapted to survive in cold environments but live in the fastest warming region on the planet. They should therefore be most threatened by climate change. We fitted a phylogenetic model of upper critical temperature ( T UC ) in 255 bird species and determined that T UC for dovekies ( Alle alle ; 22.4°C)—the most abundant seabird in the Arctic—is 8.8°C lower than predicted for a bird of its body mass (150 g) and habitat latitude. We combined our comparative analysis with in situ physiological measurements on 36 dovekies from East Greenland and forward-projections of dovekie energy and water expenditure under different climate scenarios. Based on our analyses, we demonstrate that cold adaptation in this small Arctic seabird does not handicap acute tolerance to air temperatures up to at least 15°C above their current maximum. We predict that climate warming will reduce the energetic costs of thermoregulation for dovekies, but their capacity to cope with rising temperatures will be constrained by water intake and salt balance. Dovekies evolved 15 million years ago, and their thermoregulatory physiology might also reflect adaptation to a wide range of palaeoclimates, both substantially warmer and colder than the present day.