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During an epidemiological survey following a mortality event of freshwater mussels in 2018 in the Embarrass River, Wisconsin, USA, we identified a novel microsporidian parasite in the ovaries of mucket (<i>Actinonaias ligamentina</i>), plain pocketbook (<i>Lampsilis cardium</i>), and fatmucket (<i>Lampsilis siliquoidea</i>) (Unionidae). Histopathology showed round-to-oval microsporidian spores in the cytoplasm of oocytes in 60% (3/5) of female mucket, 100% (4/4) of female plain pocketbook, and 50% (1/2) of female fatmucket. Using transmission electron microscopy, we found that mature spores were round-to-oval and measured 4.13 ± 0.64 µm (3.14–5.31) long by 2.88 ± 0.37 µm (2.36–3.68) wide. The spores had a thin electron-dense exospore with a spiky “hairy” coat, a thick electron lucent endospore, diplokaryotic nuclei, a polar vacuole, and 27–28 polar filaments arranged in 1–3 rows. Sequencing of the small subunit rRNA produced a 1356 bp sequence most similar to that of <i>Pseudonosema cristatellae</i> (92%), and phylogenetic analysis grouped it within the freshwater Neopereziida. Genetic, morphological, and ultrastructural characteristics did not closely match those of other <i>Pseudonosema</i> spp., and a new genus and species, <i>Hirsutonosema embarrassi</i> n. gen. n. sp., were designated. Additional studies could evaluate host susceptibility, distribution, seasonality, transmission, and lethal or sub-lethal effects of this parasite on freshwater mussels.