ABSTRACT Climate change is considered a key driver for shaping ecological and evolutionary processes of Arctic animals. Historical glaciation has profoundly influenced the distribution and genetic differentiation of Arctic vertebrates, and recently Arctic species are facing new and intensifying threats from rapid global warming. Understanding how past, recent and future climate change has, and will influence the evolution of Arctic animals is, therefore, crucial for effective conservation planning. Here we combine whole‐genome sequencing, demographic inference, and species distribution modeling (SDM) to assess the eco‐evolutionary responses of the gyrfalcon ( Falco rusticolus ), a resident Arctic apex predator, to climate change. Assembling a genome reference and using samples from three breeding regions across the Eurasian Arctic (Kola, Yamal, and Chukotka peninsulas), we found genetic differentiation of gyrfalcon populations from west to east, that arose during the late Pleistocene (12.9–14.7 thousand years ago (ka)) and subsequently persisted in isolation, until gene flow into the Yamal population resumed during the late Holocene. The extant gyrfalcon populations exhibit low genetic diversity, elevated inbreeding coefficients, and high genetic loads compared to the closely related saker falcon ( Falco cherrug ), and some other threatened species with small populations, likely due to a population bottleneck about 1 ka, which might compromise the long‐term viability of this Arctic raptor. Additionally, the effective population size ( N e) of the Kola gyrfalcon population was inferred to be in decline over the past 165–60 years. SDM based on ensemble models further predicts a substantial reduction of climatically suitable areas for Kola gyrfalcons under future global warming scenarios. Our study highlights how past climatic fluctuations and ongoing warming jointly shape the genomic landscape of endemic Arctic birds and provides insights into making conservation strategies for Arctic animals in a rapidly warming environment.