Sexual polymorphism, a main strategy to maintain genetic diversity within a species, has long been a major focus in biology. Notwithstanding, in plants, evolution of sexual systems and mechanisms underlying these transitions have been little unveiled. We have elucidated the molecular mechanism of sex determination in persimmons (Diospyros spp.), where the Y-encoded smRNA gene OGI can repress the female-determining gene MeGI, and also in kiwifruits (Actinidia spp.), where the Y-encoded two sex determinants, Shy Girl and Friendly Boy, control gynoecium and androecium development, respectively. Although the molecular functions of these determinants are distinct, they have common evolutionary scenarios involving transitions of sexual systems. In persimmon, a recent genome triplication (hexaploidization) in cultivated persimmon (D. kaki) derived “flexible” sexuality via establishing epigenetic layers on the two sex determinants. On the other hand, an ancient Diospyros-specific paleo-genome duplication (paleo-tetraploidization) enabled neofunctionalization in the proto-MeGI, via positive selection, to establish a new function as a sex determinant. In kiwifruit, one of the two sex determinants, Shy Girl, was derived from neofunctionalization via Actinidia-specific duplication event. These findings exemplify how plant-specific numerous duplication events can drive flexible genetic material whose variation can be selected for development of new sexual systems.