Formate is an attractive liquid carbon carrier that can be sustainably produced from carbon dioxide via electrochemical reduction, yet its utilization as the sole carbon source in eukaryotes is fundamentally constrained by inefficient energy coupling and severe stress toxicity. Here, we reprogrammed Yarrowia lipolytica into a synthetic formatotrophic yeast capable of stable growth on formate alone. Adaptive laboratory evolution yielded a strain with a biomass yield of 5.22 ± 0.12 g CDW mol⁻¹ formate, exceeding all previously reported formate-assimilating systems. Multi-omics and allelic reconstruction revealed a coupled adaptive program that redistributes ATP and reducing power, reinforces protein homeostasis via enhanced 26S proteasome assembly, and mitigates oxidative and carbonyl stress through coordinated membrane lipid remodeling and activation of the cellular integrity system. We further strengthened formate assimilation by rebalancing glycine-node flux partitioning, thereby maintaining high-throughput C1 delivery into central metabolism. Finally, integration of the evolved chassis with a copper–bismuth electrocatalyst in a near-neutral electrobiochemical system enabled the direct conversion of carbon dioxide and electrical energy into free fatty acids, establishing a mechanistically defined eukaryotic platform for formate-based CO₂ electrosynthesis