Environmental change can have drastic effects on natural populations. To successfully predict such effects, we need to understand how species that follow different life-history strategies respond to stressful conditions. Here I focus on two stressors, increased flight and dietary restriction, and their effects on bioenergetics and life-history. Using the Glanville fritillary butterfly (Melitaea cinxia), I subjected mated females to three treatments: (1) control conditions, (2) repeated forced flight with unlimited food, and (3) repeated forced flight coupled with food restriction. Interestingly, flight increased fecundity: females in both flight treatments initiated oviposition earlier, laid more egg clutches, and had higher total fecundity than control females. However, food-restriction by 50% reduced clutch size and resulted in an approximately 25% decrease in total fecundity compared to flown females with unlimited food. There were no differences in egg wet mass, water content or hatching success. Flown females with unlimited food appeared to exhibit a trade-off between reproduction and lifespan: they had higher mass-independent resting metabolic rate and shorter lifespan than females in the other treatments. Mass-independent flight metabolic rate, reflecting flight capacity, did not differ among the treatments. There were no differences in the rate of metabolic senescence across the treatments. The current findings suggest a mechanistic link between flight and reproduction, potentially mediated by juvenile hormone signalling. It appears that this wing-monomorphic butterfly does not show an oogenesis-flight trade-off often found in wing-dimorphic insects. Nevertheless, nectar-feeding is needed for achieving maximum reproductive output, suggesting that diminishing nectar resources may negatively impact natural populations.