Bowhead whales were heavily exploited during commercial whaling between the 16th and 20th centuries. Current and near-future climate warming poses a new threat. Assessing bowhead vulnerability to climatic change remains challenging due to insufficient knowledge regarding responses to past climates and pre-whaling population dynamics. We integrate paleogenomics and stable isotopes (δ13C and δ15N) from 206 bowhead fossils from the Atlantic Arctic with paleoclimate and ecological modeling based on 823 radiocarbon-dated fossils, including 140 from this study. We find long-term resilience of bowheads to Holocene environmental perturbations, with no detectable changes in genetic diversity or population structure. Simulated commercial-whaling-driven genetic and fitness changes indicate that population subdivision and loss of genetic diversity are unlikely to be fully realized, despite nearly a century since whaling ceased. Furthermore, even in simulated complete population recovery scenarios, overall fitness did not return to pre-whaling levels, potentially compromising the future resilience of bowhead whales.