Clowesia is a relatively small Neotropical genus of Orchidaceae sister to the much larger Catasetum. A hypothesis of internal relationships was proposed in the 1990s, based solely on morphological and life history characters, which so far has not been robustly tested, which is done herein. The genus encompasses seven formally described species; here, we synonymize one species, describe Clowesia arevaloi as a new species endemic to Ecuador, propose the new combination Clowesia scurra and designate lectotypes for C. dodsoniana and C. thylaciochila. Furthermore, we propose an epitype for C. glaucoglossa, and a type for Warsewitschia. We also propose a lectotype and establish the correct authorship for Warsewitschia, a hitherto ignored synonym of Clowesia. We present a phylogenetic analysis of combined molecular evidence (ITS, ETS, matK‐trnK, trnS‐G, yfc1), evaluate the evolution of reproductive characters and explore the biogeography of the genus. Our main results are: Clowesia, as well as its composing clades hypothesized in the 1990s, is monophyletic, and the relationships between species feature a divergence pattern associated with their reproductive strategies, the most important of all being the place where the pollinarium is positioned on the bee's body. Likewise, we estimate the origin of the genus in Megamexico in the Miocene; the divergence and diversification of the main clades within appears to be associated with the expansion and contraction of vegetation types, as well as the closing of the isthmus of Panama, which eventually allowed the return to the Amazon, the area where currently most species of Catasetinae are found.