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Abstract The northern temperate genusDracocephalumconsists of approximately 70 species mainly distributed in the steppe‐desert biomes of Central and West Asia and the alpine region of the Qinghai‐Tibetan Plateau (QTP). Previous work has shown thatDracocephalumis not monophyletic and might includeHyssopusandLallemantia. This study attempts to clarify the phylogenetic relationships, diversification patterns, and the biogeographical history of the three genera (defined asDracocephalums.l.). Based on a sampling of 66 taxa comprising more than 80% from extant species ofDracocephalums.l., morphological, phylogenetic (maximum parsimony, likelihood, and Bayesian inference based on nuclear ITS and ETS, plastidrpl32‐trnL,trnL‐trnF,ycf1, andycf1‐rps15, and two low‐copy nuclear markersAT3G09060andAT1G09680), molecular dating, diversification, and ancestral range estimation analyses were carried out. Our results demonstrate that bothHyssopusandLallemantiaare embedded withinDracocephalumand nine well‐supported clades can be recognized withinDracocephalums.l. Analyses of divergence times suggest that the genus experienced an early rapid radiation during the middle to late Miocene with major lineages diversifying within a relatively narrow timescale. Ancestral area reconstruction analyses indicate thatDracocephalums.l. originated in Central and West Asia and southern Siberia, and dispersed from Central and West Asia into the QTP and adjacent areas twice independently during the Pliocene. The aridification of the Asian interior possibly promoted the rapid radiation ofDracocephalumwithin this region, and the uplift of the QTP appears to have triggered the dispersal and recent rapid diversification of the genus in the QTP and adjacent regions. Combining molecular phylogenetic and morphological evidence, a revised infrageneric classification ofDracocephalums.l. is proposed, which recognizes nine sections within the genus.