Maintaining integrity of the plant cell walls is critical for plant health, however, our previous study showed that Cellvibrio, which is recognized by its robust ability to degrade plant cell walls, was enriched from the citrus rhizosphere to the rhizoplane (i.e., the root surface). Here we investigated the mechanisms underlying the rhizosphere-to-rhizoplane enrichment of Cellvibrio through genome-centric metagenomics and metatranscriptomics analyses. We recovered a near-complete metagenome-assembled genome representing a potentially novel species of Cellvibrio, herein designated Bin79, with genome size of 5.71 Mb across 11 scaffolds. Differential gene expression analysis demonstrated that plant cell wall degradation genes were repressed, whereas genes encoding chitin-degrading enzymes were induced in the rhizoplane compared with the rhizosphere. Enhanced expression of multi-drug efflux genes and iron acquisition- and storage-associated genes in the rhizoplane indicated mechanisms by which Bin79 competes with other microbes. In addition, genes involved in repelling plant immune responses were significantly activated in the rhizoplane. Comparative genomics analyses with five related Cellvibrio strains showed the importance of gene gain events for the rhizoplane adaptation of Bin79. Overall, this study characterizes a novel Cellvibrio strain and indicates the mechanisms involved in its adaptation to the rhizoplane from meta-omics data without cultivation.