The commensal species Streptococcus mitis and Streptococcus oralis are genetically diverse to a degree that challenges traditional definitions of species. This causes automatic identification based on DNA sequences or cellular extract profiles problematic. Based on an initial analysis of 266 genomes, we subjected a subset of 100 representative genomes to detailed phylogenetic, pairwise distance and gene pattern analyses. S. mitis and S. oralis constitute a continuum of clones that are genetically unique. To recognize most isolates as separate species is biologically and practically meaningless. We recommend bending the proposed similarity borders to accommodate the biological reality. Accordingly, we conclude that Streptococcus toyakuensis, Streptococcus chosunensis, Streptococcus gwangjuensis, Streptococcus humanilactis and Streptococcus hohhotensis are later heterotypic synonyms of S. mitis. Type strains of effectively but not validly published ‘Streptococcus shenyangsis’, ‘Streptococcus symci’ and ‘Streptococcus vulneris’ belong in S. mitis. Streptococcus parapneumoniae and Streptococcus nakanonensis are later synonyms of Streptococcus thalassemiae. Streptococcus downii is a later synonym of Streptococcus oralis subsp. dentisani, and the type of ‘Streptococcus halitosis’ belongs in Streptococcus oralis subsp. tigurinus. The genome sequence of the type of the recently proposed ‘Streptococcus bouchesdurhonensis’ is based on a mixed culture. Phylogenetic results and the pattern of presence/absence of accessory genes support the distinction of two subspecies of S. mitis, i.e. Sreptococcus mitis subsp. mitis subsp. nov. (type strain is NCTC 12261T) and Sreptococcus mitis subsp. carlssonii subsp. nov. (type strain is SK608=CCUG 55085T=LMG 33510T). The special population structure of the Streptococcus mitis–pneumoniae–pseudopneumoniae–thalassemiae complex renders automated classification of isolates based on average nucleotide identity or digital DNA–DNA hybridization values problematic. As an alternative, for initial taxonomic assignment, we present a whole-genome phylogeny-based method that enables phylogenetic comparison of new isolates in the context of a set of 117 well-characterized reference strains assigned to the Mitis/Sanguinis group.