Although central to understanding life-history evolution, the relationship between lifetime reproductive success and longevity remains uncertain in many organisms. In social insects, no studies have reported estimates of queens’ lifetime reproductive success and longevity within populations, despite the importance of understanding how sociality and associated within-group conflict affect life-history traits. To address this issue, we studied two samples of colonies of the annual bumblebee, Bombus terrestris audax, reared from wild-caught queens from a single population. In both samples, queens’ lifetime reproductive success, measured as either queens’ inclusive fitness or as total biomass of queen-produced sexuals (new queens and males), was significantly positively associated with queen longevity, measured from the day the first worker was produced. We suggest that a positive relationship between reproductive success and longevity was inherited from nonsocial ancestors showing parental care and maintained, at least in part, because the presence of workers buffers queens against extrinsic mortality.