Streptomycetes are Gram-positive actinobacteria largely represented in the plant root microbiota. The genetic determinants involved in the presence of Streptomyces in the rhizosphere are mostly unknown but can rely on the ability to release phytohormones, degrade plant cell-wall polysaccharides and produce specialised metabolites. Here we sequenced the genome of the rhizospheric and plant defence-stimulating strain Streptomyces sp. AgN23. We found out that it belongs to the soil and plant root dwelling S. violaceusniger clade. The genome annotation of AgN23 revealed the ability of the bacterium to synthesise auxin, a major regulator of plant development, to degrade plant cell wall with a large repertoire of carbohydrate degrading enzymes and to produce antimicrobials (rustmicin, mediomycin, niphimycin, nigericin) and plant bioactive compounds (nigericin, echosides, elaiophylin) through a set of biosynthetic gene clusters. We also found that these genomic features are well-conserved among members of the S. violaceusniger clade. In addition, AgN23 display original events of biosynthetic gene clusters acquisitions and losses which may account for its beneficial effect on plants. Taken together, our work supports the hypothesis that hydrolytic enzymes and specialised metabolites repertoires underpin the interaction of bacteria belonging to the S. violaceusniger clade with plant roots within the rhizosphere.