The first empirically supported phylogenetic hypothesis of relationships for the southern African endemic butterfly tribe Dirini is presented. Data derived from the morphology and ecology of the adults and immature stages (33 characters), and portions of the mitochondrial gene cytochrome oxidase I (COI) and the nuclear genes elongation factor 1α (EF1α) and wingless (WG) (totalling 1734 bp) were used to infer the relationships of the in-group genera. An expanded molecular dataset using four genera from the Nymphalini and Satyrini to root the tree, and three genera from the Melanitini to test the monophyly of the tribe, was analysed using parsimony and Bayesian methods. Estimates of divergence times were calculated using two fossil calibrations under a relaxed molecular clock model. The monophyly of the tribe and each in-group genus were strongly supported. Key findings are the sister-taxon relationship of Aeropetes and Tarsocera, the apparent simultaneous or nearly simultaneous radiation of four lineages, the polyphyly of the species within Torynesis, and the apparent trans-Atlantic dispersal of the ancestors of Manataria about 40 Ma. Estimates of divergence times indicate that the tribe has undergone two major radiations since its origin: the first when they left forest habitats in the mid–late Oligocene, shortly after the radiation of the grasses (Poaceae), and the second in the early-middle Pliocene, coinciding with the aridification of southern Africa and the spread of conditions that favoured C4 grasses over the C3 grasses that dirine larvae prefer to eat. The high species diversity within the tribe appears to be partly a taxonomic artefact that may have resulted from the misinterpretation of climate-related phenotypic variation within extant species. Relocation and breeding experiments should test this hypothesis.