The longhorn bee tribe Eucerini (Hymenoptera: Apidae) is a diverse, widely distributed group of solitary bees that includes important pollinators of both wild and agricultural plants. About half of the species in the tribe are currently assigned to the genus Eucera and to a few other related genera. In this large genus complex, comprising ca. 390 species, the boundaries between genera remain ambiguous due to morphological intergradation among taxa. Using ca. 6700 aligned nucleotide sites from six gene fragments, 120 morphological characters, and more than 100 taxa, we present the first comprehensive molecular, morphological, and combined phylogenetic analyses of the ‘Eucera complex’. The revised generic classification that we propose is congruent with our phylogeny and maximizes both generic stability and ease of identification. Under this new classification most generic names are synonymized under an expanded genus Eucera. Thus, Tetralonia, Peponapis, Xenoglossa, Cemolobus, and Syntrichalonia are reduced to subgeneric rank within Eucera, and Synhalonia is retained as a subgenus of Eucera. Xenoglossodes is reestablished as a valid subgenus of Eucera while Tetraloniella is synonymized with Tetralonia and Cubitalia with Eucera. In contrast, we suggest that the venusta-group of species, currently placed in the subgenus Synhalonia, should be recognized as a new genus. Our results demonstrate the need to evaluate convergent loss or gain of important diagnostic traits to minimize the use of potentially homoplasious characters when establishing classifications. Lastly, we show that the Eucera complex originated in the Nearctic region in the late Oligocene, and dispersed twice into the Old World. The first dispersal event likely occurred 24.2–16.6 mya at a base of a clade of summer-active bees restricted to warm region of the Old World, and the second 13.9–12.3 mya at the base of a clade of spring-active bees found in cooler regions of the Holarctic. Our results further highlight the role of Beringia as a climate-regulated corridor for bees.