Mentzelia section Bicuspidaria (Loasaceae) is a monophyletic group of desert ephemerals that inhabit the complex, heterogeneous landscapes of the southwestern United States and northwestern Mexico. To investigate species circumscriptions and evolutionary relationships in M. sect. Bicuspidaria, we employed phylogeny reconstructions based on DNA sequences from the plastid trnL-trnF, trnS-trnfM, ndhF-rpl32, and rpl32-trnL regions and the nuclear ribosomal ITS and ETS regions. Due to evidence of discordant relationships reconstructed from the plastid and nuclear partitions, we used coalescent-based methods in addition to concatenated data sets to estimate the species tree. Maximum likelihood reconstructions based on the combined plastid and nuclear data and coalescent-based reconstructions inferred congruent, fully-resolved species-level phylogenies of M. sect. Bicuspidaria. A monophyletic M. sect. Bicuspidaria was composed of two main clades, which corresponded to a clade of species endemic to the United States composed of M. reflexa, M. tricuspis, and M. tridentata that was sister to a clade of species at least partially distributed in Mexico, composed of M. hirsutissima and M. involucrata. Despite the unusual floral morphology of M. reflexa, molecular reconstructions placed M. reflexa sister to M. tridentata. All species of M. sect. Bicuspidaria were monophyletic, except for M. hirsutissima, which was composed of two distinct lineages and paraphyletic with respect to M. involucrata. The northern clade of M. hirsutissima from California and Baja California was sister to M. involucrata, and both, in turn, were sister to a geographically disjunct southern clade of M. hirsutissima from Baja California Sur and Cedros Island. These phylogeny reconstructions provide evidence for the inclusion of five species in M. sect. Bicuspidaria and have uncovered cryptic diversity that has been largely unrecognized. Character state reconstructions based on the phylogeny of M. sect. Bicuspidaria suggest innovative and, at times, homoplasious floral evolution.