Streptococci are an essential part of the human oral microbiome. Using ancient DNA preserved in the dental calculus of British populations, we reconstruct the evolutionary relationships between streptococci across 3,000 years. Observing high proportions of Streptococcus sp. DD04 and Streptococcus sanguinis across three methods tested, we found a competitive mapping approach is most conservative in characterizing species abundances. The resulting phylogeny offers important insights into humanity’s changing relationship with streptococci and their implications for health.