The genetic architecture of floral traits involved in the evolution of self-pollination provides a window into past processes of mating system divergence. In this study, we use two generations of crosses between highly selfing and predominantly outcrossing populations of Arenaria uniflora (Caryophyllaceae) to determine the minimum number, average dominance relationships, and pleiotropic effects of genetic factors involved in floral divergence. Comparison of the F₁ and F₂ phenotypic means with the expectations of a completely additive model of gene action revealed a primarily additive genetic basis for floral characters associated with mating system variation. The exception was flower life span, which showed partial dominance of the outcrosser phenology. In contrast to similarly divergent species, the substantial differences in flower size between these A. uniflora populations appear to involve relatively few genes of large effect (minimum number of effective factors = 2.2 ± 2.8 SE). In addition, correlations among traits in the F₂ generation indicate that pleiotropy may be an important feature of the genetic architecture of floral evolution in A. uniflora. The evolution of selfing via major modifiers of floral morphology is consistent with other evidence for ecological selection for preemptive self-pollination in A. uniflora. Analyses of the genetic basis of autonomous selfing were complicated by hybrid breakdown in both F₁ and F₂ generations. Only F₁ hybrids showed reductions in female fertility, but about 30% of F₁ and F₂ hybrids exhibited partial or complete male sterility. Male sterile flowers were characterized by short stamens, reduced petals, and a lack of protandry, as well as indehiscent anthers. This morphological breakdown mimics environmental disruptions of floral development and may result from novel genic interactions in hybrids.