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Fagus L. is a key component in temperate deciduous broadleaf forests of the Northern Hemisphere. However, its biogeographic history has not been examined under the framework of a fully resolved and reasonably time‐calibrated phylogeny. In this study, we sequenced 28 nuclear single/low‐copy loci (18 555 bp in total) of 11 Fagus species/segregates and seven outgroups. Phylogenetic trees were reconstructed using both concatenation‐based (maximum parsimony, maximum likelihood, and Bayesian inference) and coalescent‐based methods (StarBEAST2, ASTRAL). The monophyly of two subgenera (Fagus and Engleriana) and most sections was well supported, except for sect. Lucida, which was paraphyletic with respect to sect. Longipetiolata. We also found a major phylogenetic conflict among North American, East Asian, and West Eurasian lineages of subgen. Fagus. Three segregates that have isolated distribution (F. mexicana, F. multinervis, and F. orientalis) were independent evolutionary units. Biogeographic analysis with fossils suggested that Fagus could have originated in the North Pacific region in late early Eocene. Major diversifications coincided with a climate aberration at the Eocene/Oligocene boundary and the global cooling since mid‐Miocene. The late Miocene accelerated global cooling and the Pleistocene glaciations would have driven beeches into East Asia, North America, and West Eurasia. Meanwhile, range reduction and extinction in high latitudes, central Asia, and western North America converged to form the beech modern distribution pattern. This study provides a first attempt to disentangle the biogeographic history of beeches in the context of a nearly resolved and time‐calibrated phylogeny, which could shed new insights into the formation of the temperate biome in the Northern Hemisphere. [ABSTRACT FROM AUTHOR]