Taylor and Weibel's theory of symmorphosis predicts that structures of the respiratory system are matched to maximum functional requirements with minimal excess capacity. We tested this hypothesis in the respiratory system of the migratory locust, Locusta migratoria, by comparing the aerobic capacity of the jumping muscles with the morphology of the oxygen cascade in the hopping legs using an intraspecific allometric analysis of different body mass (M b) at selected juvenile life stages. The maximum oxygen consumption rate of the hopping muscle during jumping exercise scales as M b 1.02±0.02, which parallels the scaling of mitochondrial volume in the hopping muscle, M b 1.02±0.08, and the total surface area of inner mitochondrial membrane, M b 0.99±0.10. Likewise, at the oxygen supply end of the insect respiratory system, there is congruence between the aerobic capacity of the hopping muscle and the total volume of tracheoles in the hopping muscle, M b 0.99±0.16, the total inner surface area of the tracheoles, M b 0.99±0.16, and the anatomical radial diffusing capacity of the tracheoles, M b 0.99±0.18. Therefore, the principles of symmorphosis are upheld at each step of the oxygen cascade in the respiratory system of the migratory locust.