Alterations of the amount and quality of food consumed during ontogeny can affect different life-history traits, such as growth rate, developmental time, survival, adult size and fitness. Understanding the dynamics of such metabolic and energetic pathways and investments is particularly challenging in the case of holometabolous insects due to their strikingly different life-stages. Here we show how whole-life-cycle energy and mass budgets can be achieved for holometabolic insects through Dynamic Energy Budget (DEB) theory, permitting the fate of acquired and stored nutrients to be followed over a complete life cycle. We applied the DEB theory to model the whole life-cycle energetics of an endo-parasitic wasp, Venturia caenescens (Hymenoptera: Ichneumonidae). Data on embryo, larval and pupal dry weights, imago longevity and fecundity were used for assessing the goodness of fit of the model. Our model predicted connections between the growth curves of the larval and pupal stages, the number of eggs laid by the imago through time, and lifespan events such as the different developmental times of the parasitoid. The model enabled us to distinguish and follow the energy invested in eggs through income and capital reserves. The mechanisms leading to the double costs of being small - a shorter life under starving conditions and fewer eggs - were identified by running the model for varying amounts of food eaten early in life, according to host sizes. The final larval instar harvests around 60 times the energy of a recently hatched larva. Around 90 % of this energy is then used during pupation to build structure of the imago and to pay maintenance. Imagoes therefore emerge with only a small percentage of the energy stored by the last instar larvae. Our study shows that, despite being small, this percentage of energy stored during the parasitoid development has a great impact on adult fitness, the loss of which cannot be compensated for by a rich adult environment. Our model is generic and has applications for a wide range of applied and theoretical questions about insect energetics, from population dynamics in multitrophic systems to responses to climate change and life-history strategies.