ABSTRACT Chromosome partitioning precedes the division of the cytoplasm, and its evolution is linked with the positioning of the division plane. So far, bacterial chromosome biology has heavily focused on transversally dividing, free-living ones. Here, we determined the chromosome organization of three longitudinally dividing Neisseriaceae exclusively inhabiting the oral cavity of mammals. We showed that in all three multicellular bacteria the origin of DNA replication is invariably located at the host-attached (proximal) pole. Next, 3C-seq revealed loop-based folding of the ori region in Alysiella filiformis and Simonsiella muelleri . Moreover, genes involved in cell motility, piliation and signal transduction mechanisms were specifically looped when transcriptionally and translationally active cells adhered to a substrate, but not when cultured in liquid. Overall, we propose that proximal positioning of the ori and loop-based folding of its surrounding DNA may mediate localized translation of proteins involved in host colonization.