By successfully tracking individual maternal food intake and milk investment, we show that offspring gain more milk from their own mother, particularly when partner mothers are unrelated and when offspring born second experience strong competition from older pups. Unrelated partner mothers are less efficient, requiring more energy than sisters to rear communal broods of equivalent mass. Further, while unrelated partners provide more equal (but not proportional) investment in the brood, individual fitness gains from investment are much greater and more equal between sisters. Our results show that cryptic kin discrimination in maternal investment provides a strong selective advantage for the choice of close relatives as communal rearing partners, reducing costs and potential exploitation of effort when partners were closely matched.