Oaks (Quercus) comprise more than 400 species worldwide and centres of diversity for most sections lie in the Americas and East/Southeast Asia. The only exception is the Eurasian Sect. Cerris that comprises 15 species, a dozen of which are confined to western Eurasia. This section has not been comprehensively studied using molecular tools. Here, we assess species diversity and reconstruct a first comprehensive taxonomic scheme of western Eurasian members of Sect. Cerris using plastid (trnH-psbA) and nuclear (5S-IGS) DNA variation with a dense intra-specific and geographic sampling. Chloroplast haplotypes primarily reflected geographic patterns of species coevolution within Sect. Cerris and its sister section Ilex. We identified two widespread and ancestral haplotypes, and less common, locally restricted, derived variants. Signatures shared with Mediterranean species of Sect. Ilex, but not with the East Asian Cerris siblings, suggest that the western Eurasian lineage came into contact with Ilex only after the first (early Oligocene) members of Sect. Cerris in Northeast Asia had begun to radiate and move westwards. Nuclear 5S-IGS diversification patterns were more efficient for establishing a molecular-taxonomic framework and to reveal hybridization and reticulation processes. Four main evolutionary lineages were identified. The first lineage comprises Q. libani, Q. trojana and Q. afares and appears to be closest to the root of Sect. Cerris. These taxa are morphologically most similar to the East Asian species of Cerris, and to both Oligocene and Miocene fossils of East Asia and Miocene fossils of western Eurasia. The second lineage is mainly composed of the widespread Q. cerris and the narrow endemic species Q. castaneifolia, Q. look, and Q. euboica. The third lineage comprises three Near East species (Q. brantii, Q. ithaburensis and Q. macrolepis), well adapted to continental climates with cold winters. The forth lineage appears the most derived and comprises Q. suber, the cork oak, and Q. crenata. Quercus cerris and Q. trojana displayed exceptional levels of variation; Q. macrolepis and Q. euboica, previously treated as subspecies of Q. ithaburensis and Q. trojana, likely deserve an independent species status. A trend towards inter-specific crosses was detected in several taxa; however, we found no clear evidence of a hybrid origin of Q. afares and Q. crenata, as currently assumed. Phylogeographic inferences on the origin and diversification of Quercus Sect. Cerris are provided to fill an important gap in the knowledge of oak diversity and evolution.