Though it is well-known that honey bees thermoregulate during flight, the mechanisms remain controversial. Studies have reported constant metabolic rate and wing beat frequency across different air temperatures, while others found declining metabolism and wing beat frequency as air temperature rises. One confounding factor may be work-load during flight, which is challenging to control and manipulate in honey bees. To investigate how air temperature and increased power requirements affect flight metabolism, we flew foragers at 23°C and 35°C air temperatures and at air densities ranging from 21% O₂/79% N₂ to 21% O₂/79% He (1.288-0.441 kg·m^-3, normodense to heliox). Decreasing air density increases lift requirements, providing a way to test maximal aerobic performance during hovering flight. Flight metabolic rates of honey bees flown at 23°C air temperature were significantly higher than those flown at 35°C in normodense air. At 35°C air temperature, flight metabolic rate increased linearly by 1.4x as gas density decreased, and failure occurred in heliox, indicating a performance limit. In contrast, at 23°C air temperature, there was no increase in flight metabolic rate as air density decreased, and failure occurred sooner (at 0.779 kg·m^-3). At 23°C, thorax temperatures decreased linearly as air density fell, likely because helium increases convective and evaporative heat loss. Thermal performance curves for flight muscle predict these patterns, suggesting that flight muscle temperature plays a key role in determining the pattern of flight metabolic rate with changing air temperature and flight power requirements. Supported by USDA 2017-68004-26322.