Organisms show a remarkable inter–individual variation in reproductive success. The proximate causes of this variation are not well understood. We hypothesized that the ultrastructure of costly or complex tissues or organelles might affect reproductive performance. We tested this hypothesis in females of a sphecid wasp, the European beewolf, Philanthus triangulum (Hymenoptera, Sphecidae), that show considerable variation in reproductive success. The most critical component of reproduction in beewolf females is flying with paralysed honeybees, which more than double their weight. Because of the high energetic requirements for flight, we predicted that the ultrastructure of the flight–muscle mitochondria might influence female success. We determined the density of mitochondria and the density of the inner mitochondrial membranes (DIMM) of the flight muscles as well as age, body size and fat content. Only DIMM had a significant influence on female reproductive success, which might be mediated by an elevated adenosine triphosphate (ATP) supply. The variation in DIMM might result from differences in larval provisions or from an accumulation of mutations in the mitochondrial genome. Our results support the hypothesis that the organization of complex structures contributes to inter–individual variation in reproductive success.