Abstract: A group's composition is important for its success. Colonies of the spider Anelosimus studiosus appear to have responded to this pressure by evolving the ability to maintain mixtures of docile versus aggressive individuals that help colonies avoid extinction. Here we demonstrate that colony extinction events unite the optimal group composition of all colony constituents, regardless of phenotype, with that of the colony as a whole. This is because colony extinction events explain the majority of individual mortality events in A. studiosus. Through within- and across-habitat colony manipulations, we further determined that reduction in reproductive output by individuals bearing overabundant phenotypes underlies the ability of colonies to adaptively regulate their compositions. When we experimentally created colonies with an overabundance of the docile or aggressive phenotype, individuals bearing the overabundant phenotype exhibited reduced reproductive output, which helped to move colony compositions back towards their site-specific optima. Colonies displaced from their native sites continued to recreate the patterns of reproductive output that characterized their site of origin, suggesting a genetic component to this trait. Individuals thus appear to adaptively cull their reproductive output depending on their phenotype and the composition of their colony. There is also considerable parent–offspring colony resemblance in the extent to which colonies can or do track their ideal compositions. This conveys a kind of collective heritability to this trait. Together, while group selection appears to be the principal driver of ongoing selection on group composition in A. studiosus, patterns of selection among individuals within groups appear to promote colonies' ability to track their ideal mixtures.