The optimal deployment of reproductive resources by hermaphrodites to male versus female function (i.e., their sex allocation) depends directly on opportunities for mating. If hermaphrodites occur among females, selection should favor those with a male-biased allocation because increased male allocation enhances siring success when eggs are abundant. Similarly, when hermaphrodites co-occur with males, selection should favor those that bias their allocation toward their female function. We tested these predictions by allowing hermaphrodites of the plant Mercurialis annua to evolve in either the presence or absence of males. In the presence of males, hermaphrodites did not evolve, probably because they were already strongly female biased in the base population. However, hermaphrodites mating in the absence of males evolved greater male allocation, as predicted. Our results provide the first demonstration of an evolutionary response to the frequency of unisexuals in hermaphroditic sex allocation, and they verify the quantitative phase predicted by models for the transition between hermaphroditism and dioecy.