Long life is standardly assumed to be associated with high stress tolerance. Previous work shows that the copepod Tigriopus californicus breaks this rule, with longer lifespan under benign conditions found in males, the sex with lower stress tolerance. Here we extended this previous work, raising animals from the same families in food-replete conditions until adulthood and then transferring them to food-limited conditions until all animals perished. As in previous work, survivorship under food-replete conditions favored males. However, under food deprivation lifespan strongly favored females in all crosses. Compared to benign conditions, average lifespan under nutritional stress was reduced by 47% in males but only 32% in females. Further, the sex-specific mitonuclear effects previously found under benign conditions were erased under food limited conditions. Results thus demonstrate that sex-specific lifespan, including mitonuclear interactions, are highly dependent on nutritional environment.