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Oaks are dominant forest tree species widely distributed across the Northern Hemisphere, where they constitute natural resources of economic, ecological, social and historical value. Hybridisation and adaptive introgression have long been thought to be major drivers of their ecological success. Therefore, the maintenance of species barriers remains a key question, given the extent of interspecific gene flow. In this study, we made use of the tremendous genetic variation among four European white oak species (31 million single nucleotide polymorphisms (SNPs)) to infer the evolutionary history of these species, study patterns of genetic differentiation and identify reproductive barriers. We first analysed the ecological and historical relationships among these species and inferred a long-term strict isolation followed by a recent and extensive postglacial contact using approximate Bayesian computation. Assuming this demographic scenario, we then performed backward simulations to generate the expected distributions of differentiation under neutrality to scan their genomes for reproductive barriers. We finally identified important intrinsic and ecological functions driving the reproductive isolation. We discussed the importance of identifying the genetic basis for the ecological preferences between these oak species and its implications for the renewal of European forests under global warming.