For the very first time, morpho-anatomical features of both fruiting bodies as well as below-ground structures have been confronted with a newly produced multigene phylogeny of root symbiotic basidiomycetes using one of the most speciose genera of ectomycorrhizal fungi (Russula, Russulales) as an example. In this first of two papers, the authors focus more specifically on below-ground structures. Our five-gene phylogeny divides the genus in five main clades, here interpreted as representing seven subgenera, all significantly supported. Although more conserved than features of fruiting bodies, the anatomy of ectomycorrhiza does not allow for an unambiguous characterization of the main clades resolved by phylogenetic analysis, but the anatomy of ectomycorrhiza performs better to naturally classify the species of this genus. Features of fruiting bodies remain much more adequate for the delimitation of terminal clades and are irreplaceable for morphological species identification. Tropical taxa mostly nest in ancient lineages, but are also present in some terminal clades of otherwise temperate species groups. The shift from plectenchymatic to pseudoparenchymatic ECM outer mantle structures happened most likely already in the paleotropics, and is here hypothesized to have facilitated a major diversification of the genus with new hosts in the northern hemisphere. Available data as well as our own observations on below ground structures of several Lactifluus species suggests that this genus shares with Russula the absence of lactifers in ECM mantles and rhizomorphs, contrary to species of Lactarius where lactifers are always present. First observations on rhizomorphs of species in Multifurca confirm the presence of vessel-like and ladder-like hyphae, also found in the other agarioid genera of this family, while distinct lactifers are only present in the lactarioid, but not in russuloid members of this genus.