Drawing on examples from S-RNase-based self-incompatibility (SI), Slocus genealogies are used to infer the demographic history of lineages, the history of mating-system transitions in entire plant families and aspects of the evolution of the S-locus itself. Two lineages of Solanaceae suffered severe restrictions of S-locus diversity evident after millions of years. Broadly shared ancestral S-locus polymorphism is evidence that loss of this form of incompatibility was irreversible in the Solanaceae. Frequent and irreversible loss implies incompatibility is either declining in frequency through time, or that it confers an increased diversification rate relative to self-compatibility (SC). Differences in diversification rate among self-incompatible and self-compatible lineages likely cause the failure of current phylogenetic methods to correctly reconstruct the history of SI. Genealogies also show that origination of new S-RNases rarely occurs within the lifetimes of species. Surprisingly, genealogies of F-box genes purported to provide pollen specificity often do not correspond to those of their cognate S-RNases, indicating we have much to learn about how this system works and evolves.