The aim of this study was to evaluate the effect of intra-sexual competition on testosterone dynamics and the function of the stress axis in adult males of the North American red squirrel (Tamiasciurus hudsonicus), a species with a well-established scramble-competition system. Using an ACTH hormonal challenge protocol as a proxy for competitive interactions, we compared the testosterone dynamics in breeding males with that in nonbreeding males in the Yukon. To gain an integrated picture of their physiological state, we also assessed changes in their stress hormones and energy mobilization. Testosterone levels at the base bleed were high in breeding males (2.72 ng/mL) and virtually absent in non-breeding males (0.04 ng/mL). Breeding males were in better condition (heavier body mass, higher hematocrit and erythrocytes), had higher indices of immune function (neutrophil:lymphocyte ratio), but a similar ability to mobilize energy (glucose) compared with non-breeding males. Though total cortisol was higher in non-breeding males, free cortisol was twice as high in breeding males as their corticosteroid binding globulin levels were half as high. In response to the ACTH challenge, testosterone levels in breeding males declined 49% over the first hour and increased 36% over the next hour; in non-breeding males levels showed no change. Free cortisol increased only modestly (26% in breeding males; 23% in non-breeding males). Glucose levels changed similarly in breeding and nonbreeding males, declining for the first 30 min and then increasing for the next 60 min. There are four probable interrelated reasons for these patterns in male red squirrels: the marginal benefits of each mating, the constraints of mate searching away from their own resource-based territories, energy mobilization in a harsh environment, and a relatively long life span.