Fossil pollen records suggest rapid migration of tree species in response to Quaternary climate warming. Long-distance dispersal and high gene flow would facilitate rapid migration, but would initially homogenize variation among populations. However, contemporary clinal variation in adaptive traits along environmental gradients shown in many tree species suggests that local adaptation can occur during rapid migration over just a few generations in interglacial periods. In this study, we compared growth performance and pollen genetic structure among populations to investigate how populations of Sitka spruce (Picea sitchensis) have responded to local selection along the historical migration route. The results suggest strong adaptive divergence among populations (average Q(ST)=0.61), corresponding to climatic gradients. The population genetic structure, determined by microsatellite markers (R(ST)=0.09; F(ST)=0.11), was higher than previous estimates from less polymorphic genetic markers. The significant correlation between geographic and pollen haplotype genetic (R(ST)) distances (r=0.73, P<0.01) indicates that the current genetic structure has been shaped by isolation-by-distance, and has developed in relatively few generations. This suggests relatively limited gene flow among populations on a recent timescale. Gene flow from neighboring populations may have provided genetic diversity to founder populations during rapid migration in the early stages of range expansion. Increased genetic diversity subsequently enhanced the efficiency of local selection, limiting gene flow primarily to among similar environments and facilitating the evolution of adaptive clinal variation along environmental gradients.