Expression of a capsular polysaccharide is considered a hallmark of most invasive species of bacteria, including Streptococcus pneumoniae, in which the capsule is among the principal virulence factors and is the basis for successful vaccines. Consequently, it was previously assumed that capsule production distinguishes S.聽pneumoniae from closely related commensals of the mitis group streptococci. Based on antigenic and genetic analyses of 187 mitis group streptococci, including 90 recognized serotypes of S.聽pneumoniae, we demonstrated capsule production by the Wzy/Wzx pathway in 74% of 66 S.聽mitis strains and in virtually all tested strains of S.聽oralis (subspecies oralis, dentisani, and tigurinus) and S.聽infantis. Additional analyses of genomes of S.聽cristatus, S.聽parasanguinis, S.聽australis, S.聽sanguinis, S.聽gordonii, S.聽anginosus, S.聽intermedius, and S.聽constellatus revealed complete capsular biosynthesis (cps) loci in all strains tested. Truncated cps loci were detected in three strains of S.聽pseudopneumoniae, in 26% of S.聽mitis strains, and in a single S.聽oralis strain. The level of sequence identities of cps locus genes confirmed that the structural polymorphism of capsular polysaccharides in S.聽pneumoniae evolved by import of cps fragments from commensal Streptococcus species, resulting in a mosaic of genes of different origins. The demonstrated antigenic identity of at least eight of the numerous capsular polysaccharide structures expressed by commensal streptococci with recognized serotypes of S.聽pneumoniae raises concerns about potential misidentifications in addition to important questions concerning the consequences for vaccination and host-parasite relationships both for the commensals and for the pathogen.