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Sleep deprivation negatively impacts both physical and psychological health in both humans and animal models. Exercise, on the other hand, can have beneficial effects on various aspects of physical and mental health. However, little is known about the ways in which sleep deprivation and exercise may interact, especially for exceptionally high levels of exercise. We studied High Runner (HR) mice from a long-term artificial selection experiment to investigate how genetically high exercise level could impact the response to sleep deprivation. A total of 192 adult mice from four replicate HR and four non-selected Control lines (balanced for sex) completed six days of baseline wheel access, followed by three days with or without 6 h/day of total sleep deprivation (TSD) via gentle handling. As expected, HR mice ran farther and faster compared to Controls during days 1-6. TSD reduced the running distance and duration in mice from Control lines, while HR increased running speed and maintained distance (treatment × linetype interaction). TSD-induced changes in body mass differed between linetypes (treatment × linetype interaction): Controls tended to gain mass, whereas HRs lost mass. During the three days prior to TSD, HR mice consistently exhibited more active and fewer maintenance behaviors than Controls. TSD increased resting and decreased wheel activity in Controls but not HRs (treatment × linetype effects significant for both categories). These results demonstrate that genetically based high voluntary activity levels are associated with altered responses to TSD.