Egg parasitoids face unique developmental constraints. First, they have exceptionally limited resources to support themselves and their siblings through three life stages. Second, they develop within the physiological system of another species, which they modify to their own ends. We examined how these constraints affect the metabolic physiology of egg parasitism, and whether parasitoids retool their host eggshell to account for their different metabolic demands. Higher-conductance eggshells allow more oxygen to reach the developing parasitoids, but also allow more water to leave the egg. We used
Manduca sexta
(Lepidoptera: Sphingidae) eggs and
Trichogramma
(Hymenoptera: Trichogrammatidae) parasitoids from southeastern AZ, USA. Compared with unparasitized
Manduca
eggs, eggs parasitized by
Trichogramma
had lower peak metabolic rates and approximately 50 per cent lower metabolic efficiency. However, developing
Trichogramma
were far more efficient than typical transfer efficiencies between tropic levels (approx. 10%). Even within a few hours of parasitization, eggs containing more
Trichogramma
had lower per-parasitoid metabolic rates, suggesting that parasitoid larvae have mechanisms for rapidly adjusting their metabolic rates based on number of siblings. Parasitoids also appear to control the conductance of their host eggshell: their different metabolic demands were mirrored by shifts in rates of water loss.