Population genetic studies can contribute to current knowledge about the epidemiology of pathogens such as Streptococcus mutans, which is one of the most widely distributed bacteria in the world to be associated with human dental caries. In the present study, we investigated whether the population genetic structure of the species is clonal or recombinant, and we also evaluated the current levels of gene flow, admixed ancestry, and the hypothesis of an expansion of the bacteria within the last 10 000 years. Strains of S. mutans from Cordoba (Argentina) were obtained, with sequences of the genes aroE, gltA, gyrA, and lepC genes being aligned with those of strains from Japan, Thailand, and Finland. Most of our statistical analyses performed on the DNA matrix of 193 strains supported the existence of recombination at the intergene level. We also estimated the number of genetic clusters via Bayesian analyses, with three genetic clusters being detected in the four countries at different frequencies, as well as the number of strains with pure or admixed ancestry varying among countries. Argentina revealed 50% admixed strains, whereas these types of strains were present in only 8–19% of the other three countries analyzed. This result could be associated with the important human migration waves that Argentina has experienced, which may have mixed strains of S. mutans of different geographical origins. The demographic history was obtained using Extended Bayesian Skyline Plot anslysis, which showed important growth in the effective population size approximately 5000 years ago, coincident with the beginning of the dispersion of agriculture and a change to a diet rich in carbohydrates.