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 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 was reduced during a given acute flight, and b) antioxidant capacity and oxidative damage in plasma and tissues of flight-trained birds were similar to that of untrained birds. Flight-trained birds that expended more energy per unit time (kJ/min) during their longest, final flight decreased the non-enzymatic component of their antioxidant system the most during the final flight. Dietary antioxidant effect: Flight-trained birds that consumed more dietary anthocyanins had similar antioxidant capacity in liver and flight-muscle compared to untrained birds, and oxidative damage was prevented in the flight-muscle and reduced in the liver of flight-trained birds compared to untrained birds. Dietary fat quality effect: Contrary to our predictions, dietary 18:2n-6 did not influence oxidative status even after flight training. We found limited evidence that circulating and tissue-level oxidative capacity and damage were tightly regulated in flight-trained starlings, in contrast to the precise regulation on gene expression and enzyme activity that were observed in companion studies. 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.