Insects exchange respiratory gases through a gas-filled, highly branched tracheal system, that extends from paired segmental sipracles to fine tracheoles. Gas exchange between the tracheoles and the tissues is entirely diffusive, but locusts, and many other insects, rely on convection of gas within the tracheal system for facilitating gas transport from the environment to the tracheoles even at rest. In this study we compared structural and functional tracheal system traits between migratory locust (Locusta migratoria) populations originating in the Tibetan Plateau (TP; 4000 above sea level) and in low altitude Hainan Province (HP), China. We hypothesized that the TP locusts have adapted to low environmental oxygen availability in their natural habitat. Following multiple generation rearing at sea-level laboratory conditions TP locusts were significantly smaller than HP conspecifics, yet their tracheal volume was significantly higher. Mass-specific metabolic rates were similar in both populations, but gradual exposure to decreasing environmental oxygen levels yielded a more pronounced metabolic (and ventilatory) response in non-adapted HP compared with TP. Critical oxygen partial pressures, under which metabolic rates cannot be maintained, were marginally lower in TP compared with HP (1.8±0.2 and 2.4±0.2 kPa, respectively), but just short of statistical significance (p=0.07). Nevertheless, this evolved variation in respiratory system function may be more pronounced during activity, when tissue oxygen demand is higher. Moreover, exposure to hypoxic conditions throughout development resulted in lower adult body mass in HP, but not TP locusts, compared with development in normoxia, highlighting long-term effects of evolved respiratory adaptation.