Evolutionary ecologists often seek to identify the mechanisms maintaining intraspecific variation. In social animals, whole groups can exhibit between-group differences in their collective traits. We examined whether negative frequency-dependent selection (i.e., a rare-type advantage) could help to maintain between-group variation. We engineered neighborhoods of social spider colonies bearing bold or shy foraging phenotypes and monitored their fecundity in situ. We found that bold colonies enjoyed a rare-type advantage that is lost as the frequency of bold colonies in a neighborhood increases. The success of shy colonies was not frequency-dependent. These dynamics appear driven by a foraging advantage of bold colonies that is lost in bold neighborhoods because prey become scarce, and shy colonies perform better than bold colonies under low-resource conditions. Thus, to understand selection on collective traits, it is insufficient to examine groups in isolation. One must consider the phenotypic environment in which groups reside and compete.