The oyster Crassostrea gigas is a major, global aquaculture species. As with any domestically-farmed species, the characterization of breeding lines that yield desired phenotypes is of immense value. An understanding of the fundamental biological bases of such phenotypes is needed to enhance aquaculture production. The aim of our study was to investigate the mechanisms of protein metabolic dynamics and energy allocation in oyster larvae. A series of controlled crosses yielded full-sibling larval families that allowed for measurements of integrative physiological processes during development. Experimentally, phenotypic contrasts between larval families were assayed by measuring: (1) growth and survival, (2) utilization of energy reserves of lipid and protein, (3) rates of protein synthesis and turnover, (4) respiration rates, and (5) transcriptome gene expression. Initially, newly-formed 2-day-old veliger larvae from four different families had similar sizes and physiologies, as measured by respiration, protein synthesis, turnover and content, the amount of energy allocated to protein synthesis, and gene expression pattern. Upon feeding, notable phenotypic contrasts became evident in different families. The larval family with faster growth had higher rates of protein synthesis and allocated a higher percentage of available energy to that single process. Based on family-specific differences, a series of samples was selected for developmental time-course analysis of changes in RNA pools. Principal component analyses of family-specific differential gene expression, combined with measured biochemical and physiological processes, led to the identification of two ribosomal gene biomarkers for protein synthesis. Such biomarkers could be potentially valuable tools for assessing complex traits that regulate physiological state, leading to optimization of breeding programs for oyster aquaculture.