In this paper I present a cladistic evolutionary hypothesis for 83 taxa of Conophytum, a genus of leaf-succulent xerophytes endemic to South Africa and Namibia. My analysis is based primarily upon anatomical and micromorphological characters. The genus as a whole, and some of its traditional sections such as Ophthalmophyllum and Pellucida, is shown to be monophyletic, with bootstrap support, though many other branches are not well supported. Within Conophytum, nocturnal flowering and the embedded window-plant life form appear to have originated several times in separate lines of evolution. The most basally-diverging lineages in the genus are native to the Richtersveld in northern Namaqualand, suggesting an origin in that area. A trend towards the loss of anatomical adaptations to drought, such as sunken stomata, and the gain of adaptations in gross morphology, such as growth embedded in soil, is evident in many of the more recently derived lineages.