Streptomycetes are gram-positive actinobacteria largely represented in the plant root microbiota. The genetic determinants involved in the adaption of Streptomyces in the rhizosphere environment are mostly unknown but can rely on the ability to release phytohormones, degrade plant cell-wall polysaccharides, and produce specialized metabolites notably involved in microbial competition. Here, we sequenced the genome of the rhizospheric and plant defense-stimulating strain Streptomyces sp. AgN23. We found that it belongs to the soil- and plant root-dwelling S. violaceusniger clade. The genome annotation of AgN23 revealed the genetic potential of the bacterium to degrade the plant cell wall with a large repertoire of carbohydrate degrading enzymes, to synthesize auxin, a major regulator of plant development, 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 displays original events of biosynthetic gene cluster acquisitions and losses, which may account for its interaction with plants. Taken together, our work supports the hypothesis that evolution of a large set of conserved hydrolytic enzymes directed against plant polymers and specialized metabolite repertoires can mediate the adaptation of S. violaceusniger strains to the rhizospheric ecological niches. [Formula: see text] Copyright © 2023 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license .