Food-induced morphological plasticity, a type of developmental plasticity, is a well-documented phenomenon in larvae of the echinoid echinoderm, Dendraster excentricus. A recent study in our lab has shown that this morphological plasticity is associated with significant physiological plasticity for growth. The goal of the current study was to measure several aspects of protein metabolism in larvae growing at different rates to understand the mechanistic basis for this physiological growth plasticity. Larvae of D. excentricus were fed rations of 1000 algal cells ml−1 (low-fed larvae) or 10,000 algal cells ml−1 (high-fed larvae). Relative protein growth rate was 6.0 and 12.2% day−1 for low- and high-fed larvae, respectively. The energetic cost of protein synthesis was similar for the two treatments at 4.91 J mg−1 protein synthesized. Larvae in both treatments used about 50% of their metabolic energy production to fuel protein synthesis. Mass-specific rates of protein synthesis were also similar. Large differences in mass-specific rates of protein degradation were observed. Low-fed larvae had relatively low rates of degradation early in development that increased with larval age, surpassing those of high-fed larvae at 20 days post-fertilization. Changes in protein depositional efficiency during development were similar to those of larval growth efficiency, indicating that differences in protein metabolism are largely responsible for whole-organism growth plasticity. Low-fed larvae also had alanine transport rates that were 2 times higher than those of high-fed larvae. In total, these results provide an explanation for the differences in growth efficiency between low- and high-fed larvae and allow for a more integrated understanding of developmental plasticity in echinoid larvae.