The respiratory and metabolic systems of insects have been shown to exhibit developmental plasticity when exposed to alterations in oxygen availability during development. For example, adult trachea and mitochondria density in Drosophila is dependent on ambient oxygen levels experienced during larval development. Manduca sexta are large, endothermic moths that require elevated thorax temperatures for flight. Here we asked how energy demands of this endothermic insect influenced the developmental plasticity of the metabolic system under either hypoxic or hyperoxic developmental conditions. Manduca sexta were reared in either 10, 21, or 30% oxygen from the larval stage through adults. We examined the plasticity of tracheal and mitochondrial morphology and physiology of the adult moth. Hypoxic reared moths reached smaller sizes as adults while hyperoxic reared moths reached larger adult sizes compared with normoxic reared animals. Both hypoxic and hyperoxic reared moths had significantly longer pupation times than controls. Hypoxic reared moths had lower critical oxygen levels for flight compared with hyperoxic reared moths. Mitochondrial respiration rate in permeabilized flight muscle mitochondria was higher in hypoxic reared moths than in either control or hyperoxic reared moths, but this difference was not observed in isolated mitochondria. Unlike Drosophila, Manduca exhibit no developmental plasticity in mitochondrial densities or tracheal densities in response to hyperoxia and hypoxia. The developing Manduca sexta exhibits more limited plasticity in resopnse to altered oxygen when compared with other insects studied.