Over the last few decades North American flying squirrels (Glaucomys spp.) have experienced dramatic northward range shifts. Previous studies have focused on the potential effects of warming winter temperatures, yet the hypothesis that rising summer temperature had a role in these range shifts remained unexplored. We therefore sought to determine the effect of high environmental temperatures on the thermoregulation and energetics of flying squirrels in an area of the Northeast of North America with a recent species turnover. Unable to find a logistically feasible population of the northern species (Glaucomys sabrinus), we focused on Southern Flying Squirrels (G. volans). Using flow-through respirometry, we measured the relationship between metabolic rate, evaporative water loss, and body temperature at high ambient temperatures. We also measured core body temperature in free-ranging flying squirrels using temperature-sensitive data loggers. We detected no significant increase in metabolic rate up to ambient temperatures as high as 40 °C. However, evaporative water loss increased at temperatures above 36.2 °C. Free-ranging body temperature of flying squirrels followed a circadian pattern with a ~2 °C difference between active and resting phase modal body temperatures. Rest-phase body temperatures were influenced by environmental temperatures with higher resting temperatures observed on days with higher daily maximum ambient temperatures but not to an extent that energy or water costs were significantly increased during rest. We found that, due to a relatively high level of thermal tolerance, high ambient temperatures are unlikely to cause an energetic strain on Southern Flying Squirrels. However, these findings do not preclude negative impacts of high ambient temperatures on the northern species, and these may still play a role in the changing distributions of Glaucomys in North America.