Ecologically-relevant factors such as exercise and diet quality can directly influence how multifaceted physiological systems work; however, little is known about how such factors directly and interactively affect key components of the antioxidant system in multiple tissues of migratory songbirds. We tested 3 main hypotheses across three tissues in European Starlings fed diets with more or less antioxidants (anthocyanins) and long-chain omega-6 polyunsaturated fats (18:2n6) while being flight-trained in a wind tunnel. Stimulatory effect of flight: Flight-training stimulated the antioxidant system in that a) plasma oxidative damage (dROMs) was reduced during a given acute flight, and contrary to our predictions, b) antioxidant capacity (OXY or ORAC) and oxidative damage in plasma (dROMs), flight-muscle, and liver (LPO) of flight-trained birds were similar to that of untrained birds (i.e., not flown in a wind tunnel). Flight-trained birds that expended more energy per unit time (kJ/min) during their longest, final flight decreased antioxidant capacity (OXY) the most during the final flight. Dietary fat quality effect: Contrary to our predictions, dietary 18:2n-6 did not influence oxidative status even after flight training. Dietary antioxidant effect: Flight-trained birds supplemented with dietary anthocyanins did not have higher antioxidant capacity in plasma (OXY), or liver and flight-muscle (ORAC) compared to untrained birds. Counterintuitively, oxidative damage (dROMs) was higher in flight-trained supplemented birds compared to unsupplemented birds after an acute flight. In sum, the antioxidant system of songbirds flexibly responded to changes in availability of dietary antioxidants as well as increased flight time and effort, and such condition-dependent, individual-level, tissue-specific responses to the oxidative costs of long-duration flights apparently requires recovery periods for maintaining oxidative balance during migration.