show Abstracthide AbstractWe investigated phylogenetic and functional markers of niche partitioning of enigmatic members of the oral cavity, with a focus on members of the candidate phylum TM7. We used a metagenomic assembly and binning approach to recover metagenome-assembled genomes (MAGs) from the supragingival plaque and tongue dorsum of healthy individuals, and used long-read sequencing to associate TM7 MAGs with previously identified phylotypes through 16S rRNA sequence comparison. Our genomes represent prevalent and abundant lineages that lack genomic representation in the HOMD and National Center for Biotechnology Information (NCBI) genomic databases, including members of the Candidate Phyla Radiation. Using a multi-omics approach we show that oral TM7 species are split into plaque and tongue specialists, and that plaque TM7 phylogenetically and functionally associate with environmental TM7, while tongue TM7 associate with TM7 from animal guts. To assess the generality of our results we carried out read recruitment from approximately 200 tongue and 200 plaque Human Microbiome Project (HMP) samples; which confirm that the genomes we identified are prevalent, abundant, and site-specific. Our findings suggest that at least for TM7, dental plaque resembles non-host habitats, while tongue- and gut-associated TM7s are more strongly shaped by the host. In addition, our results shed light on other understudied members of the oral cavity, and allow for better genomic insight into prevalent, yet poorly understood members of the oral microbiome.