Mentzelia section Trachyphytum (Loasaceae) has 25–30 species found primarily in the western United States. Species delimitation and reconstruction of evolutionary relationships within Trachyphytum have been difficult due to restricted and continuous morphological variation. We employed phylogeny reconstructions based on morphology and DNA sequences from the plastid trnH-psbA, trnS-trnG, trnS-trnfM, ndhF-rp132, and rp132-trnL regions and the low-copy nuclear gene idh to investigate evolutionary relationships and patterns of hybridization and homoplasy among diploid species in Trachyphytum. Reconstructions indicated surprisingly high levels of genetic introgression among closely and distantly related diploids. Additionally, reconstructions based on molecular data showed that some morphological characters traditionally used to delineate groups exhibit homoplasy. However, both molecular- and morphologically-based reconstructions supported two major clades in section Trachyphytum. In agreement with prior hypotheses, the larger clade contains the taxa, M. congesta, M. desertorum, M. eremophila, M. nitens, M. pectinata, and M. thompsonii, whereas the sister clade composed of M. affinis, M. dispersa, and M. micrantha has not been previously suggested. Further, this study strengthens assertions that selected characters shared between the two annual sections, Trachyphytum and Bicuspidaria, are homoplasies.