Large social insect colonies exhibit a remarkable ability for recognizing group members via colony-specific cuticular hydrocarbon (CHC) pheromonal signatures. Previous work suggested that in some ant species colony-specific signatures are generated through a “gestalt” mechanism via the passive transfer and homogenization of CHCs across all individual members of the colony. In contrast, we demonstrate that nestmate recognition cues of worker honey bees (Apis mellifera) mature in foragers via a sequence of stereotypic age-dependent quantitative and qualitative chemical transitions, which are driven by intrinsic biosynthetic pathways. Therefore, in contrast to predictions of the “Gestalt” model, nestmate recognition cues in honey bee colonies do not represent a passive “average” signature that is carried and recognized by all colony members. Instead, specific colony members develop the relevant cues via an innately-determined developmental program that can be modulated by colony-specific social environmental factors.