The evolution of effectively sterile workers in the aculeate Hymenoptera (ants, bees and stinging wasps) requires that a female’s lifespan largely overlap that of her daughters. The evolution of long nest foundress lifespans in eusocial species from the short lifespans of solitary species is investigated. Analyses that control for phylogeny show for the first time that foundress adult lifespan increases, and first-brood offspring development time decreases, with increasing colony size, resulting in the ratio of foundress adult lifespan to worker total lifespan increasing with increasing colony size. These patterns support the hypothesis that the reproductive division of labour increases with increasing colony size, explaining the evolution of effectively sterile workers in species with large colonies. However, there is a discrete increase in foundress adult lifespan in the transition from non-eusociality to eusociality that is independent of colony size. An analysis of life history characters suggests that this increase is explained by nests being founded by multiple females and progressive feeding of larvae as they develop. A reduced rate of senescence of a dominant co-foundress may be selected as a plastic response to social status if high-risk tasks performed by subordinate co-foundresses reduce the dominant’s extrinsic mortality rate. Multiple-foundress nests in which one female is responsible for most or all the reproduction (semisociality) and in which foundresses are full sisters are favoured by haplodiploidy, perhaps explaining why eusociality is so common in the Hymenoptera. 

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