The massive numbers of sperm males transfer during a single mating are physiologically costly and the amount of sperm that can be stored is limited. Therefore, males can perform only a finite number of successive copulations without loss of fertility, and males should allocate sperm prudently. We investigated sperm availability and depletion in male black scavenger flies, Sepsis cynipsea (Diptera: Sepsidae), asking whether males adjust copula duration according to nutrition, their sperm stores, their own and their partner’s body size, as predicted by theory. We created a gradient of sperm limitation by restricting dung (their protein resource as adults) and subjecting males to a varying number of copulations. While male fertility did not depend on access to fresh dung (contrary to females), it did decline after three copulations, and more so when males were small. Larger females tended to lay more unfertilized eggs after copulating with previously mated males. However, copula duration was not influenced by a male’s number of previous copulations, and therefore apparently not by his current sperm stores. Nevertheless, copula duration varied with male size, with small males copulating longer, and with female size, as copulations lasted longer with larger females, suggesting that males are investing more sperm in larger, more fecund females. While male copula adjustments to their own nutrition and body size may be simple (proximate) physiological responses, responses to female size indicate more strategic and sophisticated sperm-allocation strategies than previously thought.