Existing data and models suggest increasing prominence of dinoflagellates and their blooms in future warmer ocean but supporting long-term data are sparse. Here, we used 18S rRNA gene sequencing to investigate sedimentary ancient dinoflagellate communities in northern South China Sea and compared them with contemporary dinoflagellate data from global oceans (TARA Oceans data) and 40 years of dinoflagellate bloom records in China. We found a continuous warming (by ~4.3°C in mean annual sea surface temperature) from 12 to 4.3 kiloyears before present (kyr BP), which caused an initial increase in the relative abundance and diversity of dinoflagellates, followed by a decrease reaching the lowest value, probably due to thermal stress. However, dinoflagellates flourished again after 4.3 kyr BP, coinciding with a rapid increase in human activities. Further analyses indicated that warming and environmental changes during the Holocene favored dinoflagellate generalists over specialists. These generalists have also been abundant throughout contemporary low- and mid-latitude regions, whereas specialists were more abundant at higher latitudes. The predominant generalist genera Noctiluca, Gymnodinium, and Prorocentrum in core sediment corresponded to taxa responsible for most dinoflagellate blooms in the contemporary China Seas over the past 40 years. The success of generalists during warmer periods suggests that dinoflagellate blooms are likely to expand geographically rather than simply shift toward high latitudes under global warming. Moreover, the homogenization of dinoflagellate communities resulting from generalist expansion may significantly reduce the complexity of marine plankton interactions and compromise ecosystem services under global warming.