Wing damage attenuates aerial performance in many flying animals such as birds, bats and insects. Insect wings are especially light in order to reduce inertial power requirements for flight at elevated wing flapping frequencies. There is a continuing debate on the factors causing wing damage in insects, including collisions with objects, mechanical stress during flight activity, and aging. This experimental study addressed the reasons for and significance of wing damage for flight in the house fly Musca domestica. We determined natural wing area loss under two housing conditions and recorded flight activity and flight ability throughout the animals' lifetime. Our data show that in animals with eventually pronounced damage, wing damage occurs on average after 6 h of flight, is sex specific and depends on housing conditions. Statistical tests show that physiological age and flight activity have similar significance as predictors for wing damage. Tests on freely flying flies showed that minimum wing area for active flight is approximately 10–34% below the initial area and requires a left–right wing area asymmetry of less than approximately 25%. Our findings broadly confirm predictions from simple aerodynamic theory based on mean wing velocity and area, and are also consistent with previous wing damage measurements in other insect species.