In the context of climate change plants have to cope with adverse conditions, among which water scarcity is a major threat for their survival. Thus, the regulatory processes of plants to face drought may differ depending on their ecological preferences. The European white oak complex is mainly formed by two species, Pedunculate (PO) and Sessile oak (SO) known to display different ecological features, particularly related to their adaptation drought stress. SO is a drought tolerant species while PO declines rapidly during moderate or intense drought stress episode. Thus, this situation provides a unique opportunity to identify (epi)genomic regions that matter for abiotic stress response and adaptation in forest trees. To investigate the strategies developed by two sympatric oaks species (Quercus robur L. and Quercus petraea (Matt.). Liebl) with different levels of drought tolerance, the transcriptome, small RNAome and methylome dynamics were analyzed under control and drought stress conditions and related to physiological characterizations. We have identified several physiological processes- i.e. cell wall remodeling- which may contribute to a better tolerance to water deprivation of Q petraea than of Q robur. In addition, we found many DNA methylation differences between both oak species. Some of them are independent of the growing conditions. Integration of the three datasets revealed genomic co-locations of potential importance for forest tree adaptation to drought stress. Data are consistent with molecular species-specific responses of oak to drought stress related to their ecological preferences.