Background <p>As adaptive organisms, parasites display remarkable diversity in their life cycles and life history strategies, reflecting evolutionary pressures to find and inhabit their hosts. The order Syndiniales (i.e., Marine Alveolates II and IV) has been detected in global waters and has gained increasing interest in metabarcoding studies as cryptic members of the plankton. However, this taxon of parasitic dinoflagellates possesses a bizarre yet unstudied life history trait, where two morphologically distinct types of dinospores are produced and released when their life cycle within the host comes to an end. In this study, we employed laboratory infection assays, flow cytometry, and comparative transcriptomics to untangle the functions of the two dinospore types in the syndinean parasite, <i>Hematodinium perezi</i>, released from their Atlantic blue crab host <i>Callinectes sapidus</i>.</p> Results <p>Micro-dinospores of <i>H. perezi</i> are infectious to juvenile blue crab hosts through waterborne transmission. The DNA content of both spore types is twice that of the ameboid trophont, suggesting dinospore stages represent different life history strategies rather than being haploid gametes. Comparative transcriptome reveals distinct profiles among life history stages, with upregulations of genes related to motility and host invasion in the dinospore stages. The expression of meiosis genes further supports the existence of a cryptic sexual cycle within the host.</p> Conclusions <p>Our results shed light on a long-standing question in the life history of a widespread group of parasitic dinoflagellates. The production of two dispersal stages is a unique adaptation of parasitic lifestyle and warrants consideration in interpretations of environmental data.</p>