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Marine alveolates (MALVs) are diverse, primarily parasitic micro-eukaryotes that significantly impact marine ecosystems. The life cycles of most MALVs remain elusive and the role of sexual reproduction in these organisms is a key question that may determine their ecological success. In this study we focus on a widespread dinoflagellate parasite of bloom-forming dinoflagellates, Amoebophrya. After infection, we identified two distinct spores, differing in size, ultrastructure, swimming behavior, lifespan, gene expression, and metabolite composition. The smaller spores serve as infectious propagules, equipped with an apical complex for host invasion. They exhibit a distinct, shorter, and straighter swimming pattern, likely optimized for an extended lifespan while enhancing dispersion and chance for host encounters. Transcriptomic analysis reveals that these smaller spores are primed for efficient protein synthesis upon initiating a new infection. Conversely, the larger spores cannot infect new hosts and are characterized by the expression of meiotic genes, underscoring their sexual nature. They have a shorter lifespan, exhibit more tortuous movement, along display condensed chromosomes, signaling readiness for mating. Interestingly, infected hosts already express meiotic genes, and a single infected host only produces progeny of the same spore type, suggesting that cell fate is determined prior to spore release. Our study provides one of the first formal demonstrations of a sexually specialized cell in MALVs. Isolating compatible strains for cross-breeding and understanding how environmental conditions favor each reproductive route are the next key questions for elucidating the ecological success of MALVs in marine waters.