Only high-quality males can bear the costs of an extreme sexual display. As a consequence, such males are not only more attractive, but they often live longer than average. Recent theory predicts, however, that high-quality males should sometimes invest so heavily in sexual displays that they die sooner than lower quality males. We manipulated the phenotypic quality of field crickets, Teleogryllus commodus, by altering the protein content of their diet. Here we show that nymphs and adult females reared on a high-protein diet lived longer than those on a low-protein diet. In contrast, adult males reared on a high-protein diet died sooner than those on low-protein diets because they invested more energy in calling during early adulthood. Our findings uphold the theoretical prediction that the relationship between longevity and sexual advertisement may be dynamic (that is, either positive or negative), depending on local conditions such as resource availability. Moreover, they caution the use of longevity as a proxy for fitness in sexual selection studies, and suggest avenues for future research on the relationship between sexual attractiveness and ageing.