Formic acid (FA) is a promising one-carbon feedstock for biorefinery, but developing efficient microbial hosts for its utilization remains challenging. This study discovers *Vibrio natriegens*'s exceptional FA tolerance and metabolic capacity. By rewiring the serine and TCA cycles to create a novel S-TCA closed loop and employing laboratory evolution, the researchers generated strains with significantly improved FA utilization. Introducing an indigoidine-forming pathway resulted in 29.0 g·L⁻¹ indigoidine production and 165.3 g·L⁻¹ formate consumption within 72 h (2.3 g·L⁻¹·h⁻¹ consumption rate). This work provides a valuable microbial chassis and design principles for industrial FA biorefinery.