We tested the adaptive stress hypothesis that male arctic ground squirrels (Urocitellus parryii) exhibit a stress response over the course of the breeding season that is characterized by increasing free cortisol concentrations, increasing mobilization of stored energy, and decreasing physical condition. We assessed the functioning of the hypothalamic-pituitary-adrenal axis by measuring cortisol levels in response to the stress of capture and in response to a hormone challenge protocol (dexamethasone suppression and adrenocorticotropic hormone stimulation). We measured blood glucose levels, free fatty acids, white blood cells, and hematocrit to assess the downstream physiological responses to cortisol. Immediately after spring emergence, male arctic ground squirrels had ample free abdominal fat and few signs of wounding. By the end of the breeding season 3 wk later, visible fat reserves were almost entirely gone, and most males had extensive wounds. Total plasma cortisol concentrations increased over this period, but so did corticosteroid-binding capacity, resulting in no change in the free cortisol response to capture. We found no significant changes in how the animals responded to our hormone challenges, contrary to our prediction that the stress axis should increase free cortisol production. Even though we found no change in the functioning of the stress axis, all of the downstream measures suggested that male arctic ground squirrels are chronically exposed to high cortisol concentrations. Over the breeding season, blood glucose increased, fat stores and circulating free fatty acids were depleted, and both hematocrit levels and white blood cell counts decreased significantly. Our data suggest that a more complex relationship between the stress axis and downstream measures of stress exists than that proposed by the adaptive stress hypothesis. We propose several nonexclusive, testable mechanisms that could explain our observations.