The effects of flight behavior on physiology and senescence may be profound in insects because of the extremely high metabolic costs of flight. Flight capacity in insects decreases with age; in contrast, limiting flight behavior extends lifespan and slows the age-related loss of antioxidant capacity and accumulation of oxidative damage in flight muscles. In this study, we tested the effects of age and lifetime flight behavior on flight capacity by measuring wingbeat frequency, the ability to fly in a hypo-dense gas mixture, and metabolic rate in Drosophila melanogaster. Specifically, 5-day-old adult flies were separated into three life-long treatments: (1) those not allowed to fly (no flight), (2) those allowed – but not forced – to fly (voluntary flight) and (3) those mechanically stimulated to fly (induced flight). Flight capacity senesced earliest in flies from the no-flight treatment, followed by the induced-flight group and then the voluntary flight group. Wingbeat frequency senesced with age in all treatment groups, but was most apparent in the voluntary- and induced-flight groups. Metabolic rate during agitated flight senesced earliest and most rapidly in the induced flight group, and was low and uniform throughout age in the no-flight group. Early senescence in the induced-flight group was likely due to the acceleration of deleterious aging phenomena such as the rapid accumulation of damage at the cellular level, while the early loss of flight capacity and low metabolic rates in the no-flight group demonstrate that disuse effects can also significantly alter senescence patterns of whole-insect performance.