Predicting the response of dinoflagellates to climate change is hampered by the lack of studies on adaptive evolution over long timescales, particularly to combined multiple concurrent stressors. Here, we examine the capacity of a harmful algal bloom-causing dinoflagellate, Prorocentrum obtusidens, to evolve in response to the individual and combined effects of elevated temperature (26°C vs. 22°C), increased pCO₂ (1000 μatm vs. 400 μatm), and high nitrogen: phosphorus ratios (180:1 vs. 40:1) through a 300-day selection experiment. We show that P. obtusidens is capable of adapting to the ongoing marine environmental changes. Elevated temperature remained the dominant driver of physiological changes, with those-selected populations exhibiting higher growth rates and maximum photosynthetic efficiency. Particulate organic carbon and nitrogen production decreased in the early stages and recovered in the late stages, owing to adaptive evolution. Nevertheless, particulate organic phosphorus production continued to decrease, whereas C:N, C:P, and N:P ratios all increased. When all long term-adapted populations were transferred back to ancestral conditions, nearly all traits shifted in the opposite direction, indicating that P. obtusidens retained its initial plasticity. Transcriptomic analysis revealed molecular evidence of adaptation to increased pCO₂, elevated temperature, high N:P ratio, and their combined effects. However, the core gene expression was not reversed when adapted populations were moved back to the control environment, suggesting that P. obtusidens underwent genetic differentiation, enabling it to adapt to future ocean environment changes over longer timescales. Our results provide new insights into the evolutionary responses of dinoflagellates to multiple environmental changes in the context of global change and shed new light on the molecular basis underlying interactions among those multiple drivers.