AbstractAimTo investigate how and when allopatric populations of a widely spread mountain bird in New Guinea, Amblyornis macgregoriae, have diversified, how they differ genetically, and how they may respond to future climate conditions.LocationNew Guinea.MethodsUsing whole‐genome resequencing data for 26 individuals of A. macgregoriae, we studied how geographically separate populations of this species have responded to past environmental change and how this may have shaped their current genomic structure. We estimated genotype–environment associations and variation in genomic offset to predict how the different populations may respond to climate change.ResultsA. macgregoriae today has six allopatric mountain populations, occupying sky‐islands with limited gene flow between them. We show that these populations fall into three distinct genetic clusters. Through genotype–environment modelling, we identified annual precipitation and seasonal and day‐to‐night temperature fluctuations as the environmental factors that explain most of the genetic variation in A. macgregoriae. By comparing current and predicted future (RCP 8.5 greenhouse gas scenario for year 2070) genomic variation, we found that the populations close to the Strickland Gorge region in Central Range are those most heavily affected by the predicted climate conditions.Main conclusionsThe A. macgregoriae populations have fluctuated in size as the glacial cycles caused their montane habitats to repeatedly expand and contract. Low gene flow between populations promoted local adaptation and increased genetic divergence, resulting in a considerable variation in their genomic offset to future climate conditions. Understanding populations' differential response to the ongoing global warming is important for conservation strategy planning, not least for the sensitive mountainous biodiversity in New Guinea.