The application of DNA data on a worldwide sampling has revolutionized the infrageneric classification of the highly diverse ectomycorrhizal genus Russula. Based on collections made in New Zealand, East Asia and North America, this study describes the new subgenus Cremeoochraceae, the ninth subgenus in Russula. Even though BLASTn of the ITS sequences suggested affinities with species of subgenera Russula and Heterophyllidiae, the phylogenetic analysis based on a five-locus DNA dataset placed the target samples in an independent major clade that is systematically equivalent to subgenus. The new subgenus shares with subgen. Brevipedum subsect. Pallidosporinae the general field habit, the unequal lamellae and the relatively small spores with inamyloid suprahilar spot and similar spore ornamentation. It differs from the latter subsection principally in the poor contents of all types of cystidioid cells and the often areolate-scurfy pileus surface composed of slender, undulating hyphal terminations with frequent subcapitate apices. Biogeographically, subgen. Cremeoochraceae shares with Multifurca, the sister genus of Lactarius, a circum-Pacific distribution pattern with the exception of South America. Both lineages lack representatives in Europe and Africa. The hypothesis proposing an African origin for the genus is considered unlikely.