C₄ photosynthesis is a complex trait that sustains fast growth and high productivity in tropical and subtropical conditions and evolved repeatedly in flowering plants. One of the major C₄ lineages is Andropogoneae, a group of ~ 1,200 grass species that includes some of the world's most important crops and species dominating tropical and some temperate grasslands. Previous efforts to understand C₄ evolution in the group have compared a few model C₄ plants to distantly related C₃ species, so that changes directly responsible for the transition to C₄ could not be distinguished from those that preceded or followed it. In this study, we analyse the genomes of 66 grass species, capturing the earliest diversification within Andropogoneae as well as their C₃ relatives. Phylogenomics combined with molecular dating and analyses of protein evolution show that many changes linked to the evolution of C₄ photosynthesis in Andropogoneae happened in the Early Miocene, between 21 and 18 Ma, after the split from its C₃ sister lineage, and before the diversification of the group. This initial burst of changes was followed by an extended period of modifications to leaf anatomy and biochemistry during the diversification of Andropogoneae, so that a single C₄ origin gave birth to a diversity of C₄ phenotypes during 18 million years of speciation events and migration across geographic and ecological spaces. Our comprehensive approach and broad sampling of the diversity in the group reveals that one key transition can lead to a plethora of phenotypes following sustained adaptation of the ancestral state.