Division of reproductive behaviour and alloparental care are key aspects of many animal societies. In cooperatively breeding species, variation in helping effort and unequal task participation are frequently observed. However, the extent to which the reproductive state of an individual affects the tasks performed during offspring care remains poorly understood. In the social spider Stegodyphus dumicola, approximately 40% of females reproduce, and mothers show extended maternal care including eggsac tending, regurgitation feeding and matriphagy, in which they are consumed by the offspring. We asked whether and to what extent virgin females participate in extreme maternal care and whether they differ from reproducing females in foraging activity. We show that virgin females contributed to all aspects of extended brood care, including regurgitation feeding and matriphagy. This suggests a physiological adaptation in virgin females to cooperative breeding, since in the subsocial Stegodyphus lineatus only mated females provide extended maternal care. Although virgin females and mothers are behaviourally totipotent, we found evidence for task differentiation as virgins engaged less in brood care and more in prey attack than mothers. High relatedness among nestmates and low probability of future reproduction in virgin helpers suggest alignment of reproductive interests between mothers and allomothers. Therefore, extreme allomaternal care by virgin helpers can be considered an adaptation to cooperative breeding in social spiders.