The evolutionary origins of the morphological and taxonomic diversity of angiosperms is poorly known. We used the genus Melianthus to explore the diversification of the southern African flora. Melianthus comprises eight species, and a phylogeny based on one nuclear and two plastid genes, as well as a morphological data set, confirmed that the genus is monophyletic. The two earliest diverging lineages are found in relatively mesic habitats, whereas the two terminal clades (an eastern and a western clade), each with three species, favor more arid habitats. The eastern clade is largely restricted to the summer-rainfall parts of southern Africa, and the western clade is found in winter-rainfall region. Molecular dating indicates a mid-Tertiary origin of the genus, with diversification of the eastern and western clades coincident with the Late Miocene-Pliocene uplift of the Escarpment mountains and the establishment of summer aridity along the west coast. The remarkably complex flowers are indicative of sunbird pollination, but many smaller birds can also visit. Speciation may be the consequence of allopatric divergence into edaphic-climatic niches. Divergence in flower and inflorescence morphology might be in response to the divergent pressures for nectar conservation in arid regions coupled with the need for signaling to avian pollinators in generally shrubby vegetation.