The repeated, independent evolution of phenotypic traits reflects adaptation to similar selective pressures. In some circumstances, parallel phenotypic evolution has a common genetic basis. Here, we investigate the types of genetic change responsible for the repeated evolution of red flowers among Ipomoea species. We identified three independent transitions from cyanidin- (blue/purple) to pelargonidin-type (red) anthocyanin pigments among Ipomoea species. The genetic basis for these transitions was examined using transgenics and gene expression assays. Using a literature survey to estimate the expected spectrum of mutation types capable of producing red flowers, we evaluated whether the observed distribution of mutation types differed from expectation. In these species, red floral pigmentation appears to be caused by the disruption of flux through the anthocyanin pathway at the same position. Results implicate tissue-specific regulatory changes in the same gene, which suggests the possibility that flower color evolved independently via the same genetic mechanism. Although multiple molecular mechanisms are capable of producing red flowers, we found a deviation between the distributions of observed and expected mutation types responsible for these evolutionary transitions. Regulatory mutations thus appear to be preferentially targeted during evolutionary change between species. We discuss possible explanations for this apparent bias.