Flying insects exhibit substantial variation in size and body proportions, influencing both locomotor performance and metabolic demands during flight. For instance, intra- and interspecific morphological variation affects wingbeat frequency and flight metabolic rate. Temperature, a key driver of developmental plasticity in most ectotherms, often produces an inverse relationship between body mass and developmental temperature. Here, we assessed the extent to which temperature-induced developmental plasticity in body mass maintains or disrupts morpho-functional relationships in the hawk moth, Manduca sexta. By manipulating developmental temperature, we generated a 7.75-fold range in body mass. As body mass increased, body proportions changed via allometric scaling, with minor size-independent effects of temperature treatment but no co-plasticity in muscle metabolic phenotype. Our findings show that plasticity impacted flight energetics through its effect on body mass. Wingbeat frequency decreased with increasing body mass, despite negative wing area allometry, a pattern that, in other studies, has resulted in no correlation between body mass and wingbeat frequency. Energy expenditure during flight increased with body mass on a thorax mass-specific basis, driven by changes in body proportions and ultimately leading to flight challenges. The limited plasticity observed in flight muscle metabolic phenotype suggests it is governed more by genetic variation than environmental factors, explaining adaptive changes in flight energetics. Overall, we conclude that plasticity in body mass and proportions affects flight energetics, leading to compromises in flight ability without accompanying plasticity in flight muscle metabolic phenotypes, which may limit muscle metabolic power.