Sexual ornaments, signaling individual quality to choosy females or rival males, often show steeper body size scaling compared to non-sexually selected traits. Theory posits such steeper body size scaling is the result of differential resource allocation, reflecting trade-offs between different components of fitness. Yet the process of resource allocation towards body size-dependent sexual ornaments has been rarely understood empirically. Using the Neotropical territorial damselfly Megaloprepus caerulatus, whose males and females carry wax-based, sex-specific white wing bands and white wing tips respectively, we investigated nutrition sensitivity and body size scaling of both traits by manipulating larval food availability and directly quantified both the fat allocated to wing ornaments and the fat reserve from which allocations are made. Both color traits exhibited sensitivity to food availability during larval development and steeper body size scaling compared to control traits. Although the absolute amount of fat invested in developing the color ornaments increased with body size, the proportion of total fat allocated to the ornaments decreased with body size, making exaggerated ornaments less affordable for smaller individuals. Our data demonstrate that measuring the proportion of resource pool from which an individual’s ornaments are derived (i.e., its affordability) is essential for understanding the maintenance of honesty of sexual signals.