Metabolic conversions allow organisms to produce essential metabolites from the available nutrients in an environment, frequently requiring metabolic exchanges among co-inhabiting organisms. Here, we applied genomic-based simulations for exploring tri-trophic interactions among the sap-feeding insect whitefly (Bemisia tabaci), its host-plants, and symbiotic bacteria. The simplicity of this ecosystem allows capturing the interacting organisms (based on genomic data) and the environmental content (based on metabolomics data). Simulations explored the metabolic capacities of insect-symbiont combinations under environments representing natural phloem. Predictions were correlated with experimental data on the dynamics of symbionts under different diets. Simulation outcomes depict a puzzle of three-layer origins (plant-insect-symbionts) for the source of essential metabolites across habitats and stratify interactions enabling the whitefly to feed on diverse hosts. In parallel to simulations, natural and artificial feeding experiments provide supporting evidence for an environment-based effect on symbiont dynamics. Based on simulations, a decrease in the relative abundance of a symbiont can be associated with a loss of fitness advantage due to an environmental excess in amino-acids whose production in a deprived environment used to depend on the symbiont. The study demonstrates that genomic-based predictions can bridge environment and community dynamics and guide the design of symbiont manipulation strategies.