Oenothera, the evening primrose genus, is a model system for studying the evolution of flowering plant reproductive biology. Members of this group vary in the species of pollinator that visit their flowers and in breeding systems, including both self-compatible (SC) and self-incompatible (SI) species. Here, we examine the evolutionary relationships among the six species of Oenothera section Kneiffia using sequences from two nuclear and four chloroplast genes. Through field studies we describe the effective pollinators for four species that had not been previously reported, and experimentally test for pollen limitation. Three of the six species are SC, and three are SI. The phylogeny strongly supports three separate transitions from SI to SC. Despite the expectation that SC species evolved the ability to self because of pollen limitation, or that pollen limitation evolves among SC species, we found no significant differences in pollen limitation between the SI and SC species in this study. Our results resolve the interspecific relationships within section Kneiffia, show that breeding systems can be quite labile, and provide evidence that transitions to self-compatibility do not always coincide with pollenlimitation.