We address the adaptive significance of female remating in the red flour beetle, Tribolium castaneum, a model system with an extreme mating system of little-to-no premating discrimination and rapid remating. In light of their specific ecology: the occupation of dried grain stores with no use of liquid water, we tested predictions of 4 nonmutually exclusive hypotheses addressing direct benefits that females may receive from mating: 1) topping off of sperm, 2) oviposition-stimulating seminal plasma, 3) ejaculate-derived nutrition, or 4) hydration by the ejaculate. By examining the female fitness consequences of exposure to differing humidity and nutrition environments and exposure to males manipulated to deliver different ejaculate products during mating, we found strong support only for the ejaculate hydration hypothesis. We also investigated the effects of promiscuity on males and found evidence that providing moisture in the ejaculate is costly. This is in contrast to the frequently found pattern of sexual antagonism in which males benefit from an elevated mating rate at a cost to female fitness. We found no evidence that short-term exposure to different humidity conditions influences either female remating behavior or male competitive fertilization success. We consider the role of T. castaneum’s ecology and mechanisms of postcopulatory sexual selection on the evolution of its mating system.