The millettioids and phaseoloids (Papilionoideae) correspond to six tribes with nearly 200 genera and over 3,000 species, including many vital crops such as soybean, adzuki, common, jicama, lima, mung and winged beans, cowpea, and pigeon pea. The position of many genera and relationships of multiple clades remains unresolved or with low support in spite of recent improvements in the phylogenetic studies of papilionoids. To resolve the relationships of these important lineages and provide a framework for evolution and diversification, we used over 500 nuclear genes to build phylogenetic trees encompassing these legumes. We sampled over 70% of genera in this group, including some of the less representative taxa with uncertain placemenets such as Antheroporum, Barbieria, Diphyllarium, Disynstemon, Herpyza, Neonotonia, and Platycyamus. Our results significantly improved phylogenetic resolution alaong backbones for most clades; however, we found high paralogous genes in various taxa such as Glycine, Teramnus, Amphicarpaea, and Dioclea, potentially indicative of ancestral hybridization or polyploidy. Moreover, gene tree discordance was clear in multiple nodes along the phylogenetic backbone with very shallow branches, suggesting a rapid expansion of these clades. Our results provide a framework for studying this group’s classification, tempo, and mode of evolution in the context of papilionoid evolution.