We investigated the process of sexual maturation in winged queens of the fire ant Solenopsis invicta, a species with two distinct forms of social organization. We found that queens of the monogynous social form (single reproductive queen per colony) differ little or not at all from queens of the polygynous form (multiple reproductive queens per colony) in weight and fat content when these are pupae or newly-eclosed adults. Furthermore, the size of a sclerotized region of the adult thorax, which is set during larval growth, does not differ between queens of the two forms. In contrast, winged queens of the two social forms differ dramatically in their physiological phenotypes once they have matured, with monogynous queens weighing more and having greater fat reserves than polygynous queens. A cross-fostering experiment revealed that the different maturation processes of queens of the two forms are induced largely by the type of colony in which a queen matures (monogynous or polygynous) rather than being due to intrinsic genetic differences between the forms. However, genetic variation at a single locus does appear to play some role in determining physiological phenotype in queens of the polygynous form, providing an example of genotype-environment interaction in the expression of these physiological traits. Differences between the social forms in the mature phenotypes that are produced constrain the reproductive options of queens, so that the characteristic social organization of a colony is perpetuated by virtue of the social environment in which new queens are reared.