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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 (that is, a rare-type advantage) could help to maintain between-group variation. We engineered neighbourhoods 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 neighbourhood increases. The success of shy colonies was not frequency dependent. These dynamics seem to be driven by a foraging advantage of bold colonies that is lost in bold neighbourhoods 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. The phenotypic environment in which groups reside and compete must also be considered.