The ecological and evolutionary dynamics of fruit color polymorphisms remain poorly known because patterns and agents of selection have rarely been identified. Here, we examine Acacia ligulata, a shrub of the Australian arid zone characterized by a red/yellow/orange aril color polymorphism. Seed production patterns over four populations and three years suggested that spatially variable selection may be acting to maintain the polymorphism: red and yellow aril color morphs each had the highest seed production in alternate sites. Seed production differences between morphs were a function of both intrinsic plant characters (fruit production) and predispersal seed predation, which affects the number of viable seeds matured per ovule. Fruit production differences are hypothesized to result from a genotype-by-environment interaction, perhaps related to plant vigor. In contrast, morph differences in the numbers of viable seeds per ovule are produced via differential seed predation by heteropteran insects, as demonstrated by exclusion experiments. Because these predators feed when aril color is not visible, differential predation is evidently a response to pleiotropic effects of fruit color alleles. We suggest that such pleiotropic effects may be a common feature of fruit color polymorphisms, and that the most obvious selective agents (that is, seed dispersers) may not always be the most important.