AbstractThe Arctic is among the most climatically sensitive environments on Earth, and the disappearance of multiyear sea-ice in the Arctic Ocean is predicted within decades. As apex predators, polar bears are sentinel species for addressing the impact of environmental variability on Arctic marine ecosystems. By integrating genomics, isotopic analysis, morphometrics, and ecological modelling, we investigate how Holocene environmental changes affected the evolutionary ecology of polar bears around Greenland. We show that throughout the last ∼11,000 years, Greenlandic polar bears have been heavily influenced by changes in sea-surface temperature (SST) and sea-ice cover. Most notable are major reductions in effective population size at the beginning of the Holocene and during the Holocene Thermal Maximum ∼6 kya, which coincide with increases in annual mean SST, reduction in sea-ice covers, declines in suitable habitat, and shifts in suitable habitat northwards. Furthermore, we show how individuals sampled from west and east Greenland are genetically, morphologically, and ecologically distinct. We find bears sampled in west Greenland to be larger, more genetically diverse and have diets dominated by ringed seals, whereas bears from east Greenland are smaller and less diverse with more varied diets, putatively driven by regional biotic differences. Taken together, we provide novel insights into the vulnerability of polar bears to environmental change, and how the Arctic marine ecosystem plays a vital role in shaping the evolutionary and ecological trajectories of its inhabitants.TeaserMultivariate investigations of the environment’s role in the evolutionary ecology of Greenlandic polar bears.