Eusocial hymenopteran males have exceptionally high levels of ejaculate quality, which are assumed to result from extreme selection pressures for pre- and postcopulatory male–male competition and the necessity to retain viable sperm after years of storage in female (queen) spermathecae. We hypothesized that the production of high-quality sperm carries substantial costs so that fertility of males may be compromised by stress factors when they are operating at their physiological limits. To test this, we performed a series of experiments using honeybees as our model system, to establish possible effects of male age on sperm quality and to evaluate effects of elevated temperatures, food deprivation during sexual maturation, and immune challenges. We found that sperm viability decreases with male age but that males of some colonies were better able to delay ejaculate senescence than others. Exposure to elevated temperatures and wounding both significantly decreased male fecundity, but protein deficiency after hatching did not. This suggests that investment in drones is completed at pupation and that sexual maturation does not require additional protein feeding. The sensitivity of drone fitness to stress factors related to temperature and immune system activation illustrates that hygienic monitoring and active thermoregulation by workers are essential for colony-level reproductive success. These results underline that honeybee drones have been under strong selection for extreme specialization on reproductive performance and that this precludes any exposure to the stressful conditions that foraging workers normally experience.