Abstract Certain beneficial bacteria of the root-associated microbiome such as Bacillus velezensis protect plants against diseases and are promising biocontrol agents exploited in sustainable agriculture. Unveiling the molecular dialogue governing mutualistic interactions between these beneficials and their host is essential to better understand their ecological behavior and to optimize their use as bioprotectants. However, the chemical diversity and functionality of mediators involved in this interkingdom crosstalk remain largely unexplored. In this study, we uncover a strategy by which B. velezensis exploits the root cell wall polymer pectin to prime its host for enhanced resistance against phytopathogens and to ensure a safe environment enabling its efficient root establishment. Thanks to the activity of its two conserved pectinolytic enzymes, the bacterium generates a specific pattern of short oligogalacturonides that act as efficient triggers of plant systemic defense against leaf pathogens. Moreover, these oligomers induce only weak immune responses in root cells and dampen local defense reaction in response to the perception of the bacterium itself. Our data emphasize the key role of short oligogalacturonides as mediators in the intricate interplay between plants and their bacterial associates, providing new insights into the mechanisms that enable beneficial bacteria to coexist with their host plant.