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Background  The increasing availability of microbial genomes and environmental shotgun metagenomes provides unprecedented access to the genomic differences within related bacteria. The human oral microbiome with its diverse habitats and abundant, relatively well-characterized microbial inhabitants presents an opportunity to investigate bacterial population structures at an ecosystem scale.    Results  Here, we employ a metapangenomic approach that combines public genomes with Human Microbiome Project (HMP) metagenomes to study the diversity of microbial residents of three oral habitats: tongue dorsum, buccal mucosa, and supragingival plaque. For two exemplar taxa,  Haemophilus parainfluenzae  and the genus  Rothia , metapangenomes reveal distinct genomic groups based on shared genome content.  H. parainfluenzae  genomes separate into three distinct subgroups with differential abundance between oral habitats. Functional enrichment analyses identify an operon encoding oxaloacetate decarboxylase as diagnostic for the tongue-abundant subgroup. For the genus  Rothia , grouping by shared genome content recapitulates species-level taxonomy and habitat preferences. However, while most  R. mucilaginosa  are restricted to the tongue as expected, two genomes represent a cryptic population of  R. mucilaginosa  in many buccal mucosa samples. For both  H. parainfluenzae  and the genus  Rothia , we identify not only limitations in the ability of cultivated organisms to represent populations in their native environment, but also specifically which cultivar gene sequences are absent or ubiquitous.    Conclusions  Our findings provide insights into population structure and biogeography in the mouth and form specific hypotheses about habitat adaptation. These results illustrate the power of combining metagenomes and pangenomes to investigate the ecology and evolution of bacteria across analytical scales.    Supplementary Information  The online version contains supplementary material available at 10.1186/s13059-020-02200-2.

Metapangenomics of the oral microbiome provides insights into habitat adaptation and cultivar diversity