Global warming leads to a sustained increase in sea surface temperature, which is expected to have profound impacts on the ecological functions and evolutionary trajectories of marine microorganisms. The abundant cyanobacterium Prochlorococcus accounts for ~4 Gt C of annual net primary production, yet its long‑term adaptive capacity remains unknown. In this study, we established a long-term experimental evolution system of Prochlorococcus under elevated temperature conditions. Starting from a single ancestral cell, populations were continuously cultured for 785 days at 24, 28, and 30 °C, accumulating more than 400 generations in total and ultimately yielding 187 independent evolutionary lines. The mutation rate increased with temperature, shifting from an AT to a GC bias, suggesting enhanced genomic stability. Multi‑omics revealed that warming selected mutations in six genes, collectively enhancing photosynthesis, mitigating oxidative stress, and reconfiguring central carbon metabolism to reduce biosynthetic resource expenditure. Based on experimentally measured cell-specific rates, we project that by 2100, Prochlorococcus could increase both its net primary production and oxygen release by ~46%, implying a potentially significant contribution to future marine ecosystem stability. These findings challenge the view that warming uniformly reduces its contribution to ocean biogeochemistry, revealing an unappreciated adaptive capacity in this key microbe.