Spore sacs and free spores of a metchnikovellid were found in archigregarines Selenidium sp. isolated from polychaetes Travisia forbesii. The studied worms were collected in the subtidal areas of the Kandalaksha Gulf of the White Sea and
of Zelenetskaya Bay of the Barents Sea. Spore sacs of these hyperparasites had an elongated shape with a slight flexion. They had one polar plug and contained 12–14 rounded spores. Both spore sacs and free spores were in direct contact with the cytoplasm of the host cell. Contrary to a canonical idea about development of metchnikovellids, sac-bound sporogony was often observed in this parasite without traces of ongoing free sporogony. A combination of morphological features and host range distinguishes the studied isolates from any known genus and species of metchnikovellids. Phylogenetic analysis based on the SSU rRNA gene and BUSCO phylogenomics, showed that studied isolates form a new lineage of metchnikovellids. We proposed a new genus Mesnilia gen. nov. and described a new species, Mesnilia travisiae sp. nov. (Microsporidia: Metchnikovellida) to accommodate these organisms. Phylogenetic analysis showed that there is a mixed metchnikovellid infection in the population of polychaetes T. forbesii from Zelenetskaya Bay. We found molecular evidence for presence of the second metchnikovellid species in this host, which has yet to be characterised at the morphological level. In phylogenetic and phylogenomic trees, this ‘cryptic’ parasite grouped with another new metchnikovellid discovered in the populations of Pygospio elegans collected in Zelenetskaya Bay. New isolates described in this paper form two new lineages in the phylogenomic tree of metchnikovellids. This study confirmed widespread occurrence of mixed metchnikovellid infections in infrapopulations of gregarines from polychaetes.