The Dungeness crab Metacarcinus magister supports a large and valuable fishery along the west coast of North America. Since 1998, Dungeness crabs exhibiting pink- to orange-colored joints and opaque white musculature have been sporadically observed in low prevalence from the Fraser River delta of British Columbia, Canada. We provide histological, ultrastructural, and molecular evidence that this condition is caused by a new microsporidian parasite. Crabs displaying gross symptoms were confirmed to have heavy infections of ovoid-shaped microsporidian spores (~1.8 × 1.4 µm in size) within muscle bundles of the skeletal musculature. The parasite apparently infected the outer periphery of each muscle bundle, and then proliferated into the muscle fibres near the centre of each infected bundle. Light infections were observed in heart tissues, and occasionally spores were observed within the fixed phagocytes lining the blood vessels of the hepatopancreas. Transmission electron microscopy (TEM) revealed multiple life stages of a monokaryotic microsporidian parasite within the sarcoplasm of muscle fibres. Molecular analysis of partial small subunit rRNA sequence data from the new species revealed an affinity to Ameson, a genus of Microsporidia infecting marine crustaceans. Based on morphological and molecular data, the new species is distinct from Nadelspora canceri, a related microsporidian that also infects the muscles of this host. At present, little is known about the distribution, seasonality, and transmission of A. metacarcini in M. magister.