Levels of diversity vary strikingly among different phylogenetic lineages of ants. Rapid radiations in early ant evolution have often proven difficult to resolve with traditional Sanger-sequencing data sets of modest size. We provide a phylogenomic perspective on the evolution of the hyperdiverse ant tribe Crematogastrini by analyzing sequence data for nearly 1800 ultraconserved element (UCE) loci from 153 species comprising 56 genera. We reconstruct a next-to-complete genus-level phylogeny using concatenated maximum-likelihood and species-tree approaches, estimate divergence dates and diversification rates for the tribe, and investigate the evolution of nest sites. Our results show ten well-supported major clades which we define as the Cataulacus, Carebara, Vollenhovia, Podomyrma, Crematogaster, Mayriella, Lordomyrma, Myrmecina, Paratopula, and Formicoxenus genus-groups. These lineages are estimated to have arisen from a Paleotropical ancestor (crown-group age ~75 Ma) over a relatively short time interval (50–70 Ma). The Afrotropical and especially the Indomalayan regions appear to have played a key role in the early diversification history of the tribe. Several shifts in diversification rates were found to be related to the evolution of large, widespread genera; however, associating these shifts with evolutionary innovations or events was not possible. Arboreal habitats have been successfully colonized by only few clades within Crematogastrini from ground-nesting ancestors, with no reversals supported. Our genus-level phylogeny for Crematogastrini provides insights into the diversification and evolution of one of the most diverse clades of ants, and our division of the tribe into well-supported genus-group lineages sets the stage for more detailed species-level investigations.