Nutrient availability, along with light and temperature, drives marine primary production. The ability to migrate vertically, a critical trait of motile phytoplankton, allows species to optimize nutrient uptake, storage, and growth. However, this traditional view discounts the possibility that migration in nutrient-limited waters may be actively modulated by the emergence of energy-storing organelles. Here, we report that bloom-forming raphidophytes harness energy-storing cytoplasmic lipid droplets (LDs) to biomechanically regulate vertical migration in nutrient-limited settings. LDs grow and translocate directionally within the cytoplasm, steering strain-specific shifts in the speed, trajectory, and stability of swimming cells. Nutrient reincorporation restores their swimming traits, mediated by an active reconfiguration of LD size and coordinates. A mathematical model of cell mechanics establishes the mechanistic coupling between intracellular changes and emergent migratory behavior. Amenable to the associated photophysiology, LD-governed behavioral shift highlights an exquisite microbial strategy toward niche expansion and resource optimization in nutrient-limited oceans.