The black-lipped pearl oyster (Pinctada margaritifera) is extensively farmed in French Polynesia to produce black pearls. For a sustainable management of marine resources, studying interactions between organisms and environment, and the associated factors and processes that will impact their life cycle and thus modulate population dynamics is a major research priority. Here, we describe black-lipped pearl oyster energy acquisition and use, and its control by temperature and food concentration within the Dynamic Energy Budget (DEB) theory framework. The model parametrization was based on literature data and a specific laboratory experiment. Model validation was carried out thanks to historical in-situ datasets and a dedicated field survey. Three theoretical environmental scenarios were built to investigate the response of the pearl oyster to environmental variations. We successfully modeled a wide range of life-stage-specific traits and processes, especially the delayed acceleration of growth after settlement. Applying the model on field data collected at three different culture sites required only one free-fitted parameter, the half saturation coefficient Xk, which controls how ingestion depends on food density. Xk integrates all variations linked to the trophic environment. Analysis of the kinetics of energy fluxes under theoretical environmental scenarios suggests that temperature variations induce seasonality of reproduction in a species thought to spawn opportunistically throughout the whole year. The major influence of food concentration fluctuations on growth rate and reproductive effort is highlighted. The model showed the lower performances associated with recovery time between food-rich and starvation periods. The implications of these findings in the context of black pearl farming in a changing environment are discussed.