Latitudinal and elevational gradients provide valuable experimental settings for studies of the potential impact of global warming on forest tree species. The availability of long-term phenological surveys in common garden experiments for traits associated with climate, such as bud flushing, for sessile oaks (Quercus petraea), provides an ideal opportunity to investigate this impact. We sequenced 18 sessile oak populations, and used available sequencing data for three other closely related European white oak species (Q. pyrenaica, Q. pubescens, Q. robur), to explore the evolutionary processes responsible for shaping the genetic variation across latitudinal and elevational gradients in extant sessile oaks. We used phenotypic surveys in common garden experiments and climatic data for the population of origin, to perform genome-wide scans for population differentiation, genotype-environment (GEA) and genotype-phenotype associations (GPA). The inferred historical relationships between Q. petraea populations suggest that interspecific gene flow occurred between Q. robur and Q. petraea populations from cooler or wetter areas. A genome-wide scan of differentiation between Q. petraea populations identified SNPs displaying strong interspecific relative divergence between these two species. These SNPs followed genetic clines along climatic or phenotypic gradients, providing further support for the likely contribution of introgression to the adaptive divergence of Q. petraea populations. Overall, the results of this study indicate that adaptive introgression of Q. robur alleles has occurred. We discuss the results of this study in the framework of the post-glacial colonization scenario, in which introgression and diversifying selection have been proposed as essential drivers of Q. petraea microevolution.