Sperm have traditionally been regarded as energetically cheap and effectively limitless in supply, although evidence conflicting with this view has become increasingly abundant. For instance, males from a variety of taxa have been shown to strategically partition sperm across ejaculates in response to perceived sperm competition risk. It follows that males might also be predicted to adaptively modulate the rate at which sperm are produced. Here we show that, in the giant sperm producing fruitfly Drosophila bifurca, solitary males with infrequent access to females produce sperm at a much lower rate than males raised in association with females and other males. Our results support the prediction that males with little risk of sperm competition risk or few mating opportunities should divert resources away from gamete production.