The parasitic dinoflagellates in the genus Amoebophrya infect and kill a number of free-living dinoflagellates. The parasitoid has the potential to regulate harmful dinoflagellate blooms due to its high offspring production rates and a certain degree of host specificity. The planktonic dinoflagellate Prorocentrum donghaiense Lu is a commonly observed harmful algal species in coastal waters of China, and limited studies have been conducted to explore the ecological roles of parasitism in association with bloom dynamics. Thus, the in situ occurrence, prevalence, and dynamics of Amoebophrya during the recurrent blooms of P. donghaiense were systemically studied via morphological observations and high-throughput sequencing. The parasitic infections were identified microscopically in six dinoflagellate taxa with prevalence up to 5.13%, while Amoebophrya infection in the bloom-forming species P. donghaiense was rare (<0.01%), suggesting that P. donghaiense was free of the top-down control of Amoebophrya in the area. In addition, high-throughput sequencing of environmental DNA revealed that Amoebophrya co-dominated both the initiation and termination stages of the P. donghaiense bloom (up to 21.20% of OTU), but was less abundant during persistence of the bloom (3.70% of OTU). Further, the dynamics of Amoebophrya in the water column possessed similar patterns as revealed by qRT-PCR, in which high copy numbers of Amoebophrya (up to 3.60 × 109 copies L−1) were detected in the initiation and termination stages of the P. donghaiense bloom and low copy numbers (1.16 × 109 copies L−1) during persistence of the bloom. These findings manifested the paradoxical dynamics and complicated ecological strategies of Amoebophrya organisms during dinoflagellate blooms that need further study.