Global oceans face concurrent warming, acidification, and eutrophication‑driven nitrogen‑phosphorus (N/P) imbalance, threatening coastal ecosystems and amplifying harmful algal blooms (HABs). While short-term physiological plasticity is well documented, whether prolonged warming drives heritable adaptive evolution in dinoflagellates under combined climate stressors remains unresolved, limiting predictive capacity for future HABs. we report a 300-day multigenerational selection experiment on the HAB-forming dinoflagellate Karenia mikimotoi t under warming, elevated CO₂ and high nitrogen‑phosphorus ratios. We demonstrate that warming triggers stage‑dependent physiological reprogramming: initial growth inhibition reverses over successive generations, accompanied by progressive recovery of photosynthetic efficiency and reduced oxidative stress. Time‑series transcriptomics reveal a clear temporal shift from acute stress defense toward stable metabolic homeostasis, with persistent rewiring of carbon, nitrogen, and energy metabolism. Reciprocal transplant and thermal gradient experiments confirm genetically fixed thermal adaptation, with evolved lines exhibiting an upward shift in thermal optima (22 °C to 26 °C) and enhanced heat tolerance. Temperature explains most of transcriptomic variation, acting as the dominant selective force, while elevated CO₂ and high N/P function as synergistic modulators of thermal adaptation. Our findings establish that prolonged warming drives rapid heritable adaptation in marine dinoflagellates, with profound implications for harmful algal bloom dynamics and coastal ecosystem resilience under global climate change.