Dinoflagellates, represent one of the most diverse and ecologically significant phytoplankton groups, distributed across the global ocean from polar to tropical regions, with particular abundance in subtropical and tropical seas. Despite their remarkable adaptive capabilities to temperature variability, the molecular and physiological mechanisms underlying dinoflagellate thermal adaptation remain elusive. Here, we investigated temperature preferences and molecular signatures of dinoflagellates in the subtropical and tropical seas through integrative analyses of the Tara Oceans and Bio-ORACLE databases, combined with field surveys in Daya Bay—a subtropical ecosystem subject to long-term thermal discharge. We developed a novel approach to estimate the in situ optimal growth temperature of marine phytoplankton. Our analyses reveal that dinoflagellates possess higher optimal growth temperatures than co-occurring diatoms. Metatranscriptomic profiling further indicates that under warming conditions, dinoflagellates prioritize immediate energy mobilization, enhance thiamine and housekeeping protein synthesis, suppress oxidative stress, and activate programmed cell death pathways—collectively facilitating rapid population turnover. These findings elucidate the thermal adaptation strategies of marine dinoflagellates and provide a mechanistic basis for predicting their responses to future ocean warming.