The winter mushroom, or Enokitake, is economically important and commercially cultivated on a large scale in East Asia. However, the phylogeny and species delimitation of the winter mushroom genus (Flammulina) have not been fully clarified. In this study, 81 collections of Flammulina from East Asia, Europe, and North America were studied, and their phylogeny and species delimitation were inferred from partial sequences of the ITS, tef1-alpha, rpb2, and homeodomain1 (HD1) of the mating gene (labeled as HD1-A). Genetic structure analyses based on genomic SSR markers and haplotype network analysis based on HD1-A were also used to delimit several closely related taxa. Twelve phylogenetic species were recognized, which was largely consistent with previous studies. However, our integrated studies indicated that Enokitake is not identical to the European winter mushroom Flammulina velutipes, and thus should be treated as a separate species, namely Flammulina filiformis. All cultivated strains of "F. velutipes" in East Asia, including those from South Korea and Japan with genome sequences labeled as such, are in fact F. filiformis. A new species, Flammulina finlandica, was also unexpectedly discovered in Northern Europe. Morphological descriptions of these two species, color photos of their fresh basidiomata, and line drawings of their microscopic features are presented.