Many dinoflagellate species form harmful algae blooms (HABs), the demise of which may be attributed to viral lysis. However, the activities of the bloom dinoflagellate and the infecting viruses and the interaction of the two life forms in the course of the bloom are poorly understood and underexplored. Here, we employed the metatranscriptomic data on two bloom events of Prorocentrum shikokuense to address the question. We found that the viruses that infected the plankton cells in the bloom waters were dominated by Mimiviridae and Phycodnaviridae, and the viruses might switch their infection mode during the bloom of dinoflagellate, with chronic infection appearing to be the major mode during prolonged blooms. Furthermore, we found that viruses may intervene in host organelle utilization-related processes through periodic polymorphic variants to ensure the persistence of chronic infection. These findings provide insights into dinoflagellate-viral interactions and enhance the understanding of the formation of niche dominance in dinoflagellates during HAB outbreaks.