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 a new subgenus Cremeo-ochraceae, the ninth subgenus of 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 taxonomically equivalent to subgenus. This multilocus analysis also obtained support for the recognition of two superclades in Russula, opposing subgenera Glutinosae, Archaeae and Compactae to the rest of the genus. The type species of the new subgenus is R. cremeo-ochracea from New Zealand, which is here epitypified, and the authors describe a new variety for it: R. cremeoochracea var. myrtacearum. The new subgenus also harbors a North American R. cf. inopina and its Asian counterpart, discovered from southwestern China, described here as R. estriata sp. nov. Two environmental ITS sequences, one from Japan and one from Malaysia may represent two more undescribed taxa. 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. Cremeo-ochraceae shares with Multifurca, another small relict lineage of Russulaceae, a circum-Pacific distribution pattern except for South America. Both lineages lack representatives in Europe and Africa. The hypothesis proposing an African origin for the genus is considered unlikely. Citation: Buyck B, Horak E, Cooper JA, Wang XH (2024). Introducing Russula subgen. Cremeo-ochraceae, a new and very small lineage sharing with Multifurca (Russulaceae) an identical, largely circum-Pacific distribution pattern. Fungal Systematics and Evolution 14: 109-126. doi: 10.3114/fuse.2024.14.07.