Wing-dimorphism in crickets is maintained by a resource allocation-based trade-off between flight and oogenesis. Flightless short wing (SW) crickets preferentially divert nutrients to ovaries to support oogenesis, while flight capable long wing (LW) crickets divert nutrients to somatic maintenance to support metabolically active flight muscles and accumulate energy stores that fuel flight. Although the underlying metabolic basis of the flight-oogenesis trade-off is well characterized, we do not know whether the distinct physiological demands of flight and reproduction also drive shifts in resource acquisition and energy production capacity. We integrate data from two separate experiments, showing how resource acquisition (feeding behavior), allocation (tissue growth), and energy production capacity (mitochondrial function) change throughout the lifecycle. At the start of adulthood, SW crickets initiated rapid oogenesis and increased protein intake. However, when feeding on a protein-deficient diet ovarian synthesis by SWs was reduced, suggesting that without sufficient protein acquisition, biosynthetic demands of oogenesis could no longer be met. Additionally, a decline in mitochondrial energy production capacity accompanied the completion of ovarian synthesis by SWs on the seventh day of adulthood. LW crickets consumed carbohydrate-rich diets and mitochondrial function changed dynamically across adulthood. LW mitochondrial capacity for energy production peaked at the time of dispersal, but rapidly declined following loss of flight-capability. Together, this suggests that behavioral and physiological plasticity in resource acquisition and energy production have evolved along with life histories to enable shifts in resource allocations.