The relationship between whole-organism growth and metabolism is generally assumed to be positive and causative; higher metabolic rates support higher growth rates. In Manduca sexta, existing data demonstrate a deviation from this simple prediction: at supraoptimal temperatures for larval growth, metabolic rate keeps increasing while growth rate is decreasing. This mismatch presumably reflects the rising “cost of maintenance” with temperature. Precisely what constitutes this cost is not clear, but we suspect the efficiency with which mitochondria harness oxygen and organic substrates into cellular energy (ATP) is key. We tested this by integrating existing data on M. sexta growth and metabolism with new data on mitochondrial bioenergetics across the temperature range 14°–42°C. Across this range, our measure of mitochondrial efficiency closely paralleled larval growth rates. At supraoptimal temperatures for growth, mitochondrial efficiency was reduced, which could explain the mismatch between growth and metabolism observed at the whole-organism level.