Shifts in flower symmetry have occurred frequently during the diversification of angiosperms, and it is thought that such shifts play important roles in plant-pollinator interactions. In the model developmental system Antirrhinum majus (snapdragon), the closely related genes CYCLOIDEA (CYC) and DICHOTOMA (DICH) are needed for the development of zygomorphic flowers and the determination of adaxial (dorsal) identity of floral organs, including adaxial stamen abortion and asymmetry of adaxial petals. However, it is not known whether these genes played a role in the divergence of species differing in flower morphology and pollination mode. We compared A. majus with a close relative, Mohavea confertiflora (desert ghost flower), which differs from Antirrhinum in corolla (petal) symmetry and pollination mode. In addition, Mohavea has undergone a homeotic-like transformation in stamen number relative to Antirrhinum, aborting the lateral and adaxial stamens during flower development. Here we show that the patterns of expression of CYC and DICH orthologs have shifted in concert with changes in floral morphology. Specifically, lateral stamen abortion in Mohavea is correlated with an expansion of CYC and DICH expression, and internal symmetry of Mohavea adaxial petals is correlated with a reduction in DICH expression during petal differentiation. We propose that changes in the pattern of CYC and DICH expression have contributed to the derived flower morphology of Mohavea and may reflect adaptations to a pollination strategy resulting from a mimetic relationship, linking the genetic basis for morphological evolution to the ecological context in which the morphology arose.