This study discovered the first Asian population of Sphaeroforma nootkatensis (SphX), a member of Mesomycetozoea, in the southern coastal region of South Korea. Although investigating parasites in Pacific oysters (Crassostrea gigas), a single-cell microorganism was isolated from gill tissues. Comprehensive phylogenetic analysis of its 18S rDNA revealed its placement within the order Ichthyophonida, class Mesomycetozoea. SphX formed a distinct cluster within Sphaeroforma spp., separate from Pseudoperkinsus tapetis. Morphological examinations of in vitro cultured cells revealed two distinctive life stages characterized by multilobe and granular sporangium, accompanied by corresponding non-motile larger and motile smaller endospores, respectively. Scanning electron microscope analysis depicted lobular and smooth surfaces on vegetative cells, indicative of differing life cycle stages. Transmission electron microscope observations revealed intriguing features consistent with previous reports on Mesomycetozoea. A prominent fibrillar structure was noted in a vegetative cell. In contrast, smaller endospores were observed with cilia-like structures surrounding the cell wall, indicating their mode of movement. The Ray's fluid thioglycollate medium assay showed that SphX cells were digested, whereas some small endospores remained resistant. This discovery provides novel insights into the life stages of Mesomycetozoans and geographical distribution and underscores the importance of monitoring oyster health for effective aquaculture management.