To increase agriculture sustainability, this study addresses the demand for herbicide-resilient plant growth-promoting (PGP) bacteria. A bacterial culture collection of 120 high herbicide concentration tolerant (HHCT) strains from S-metolachlor-treated soils was generated that was able to grow on and use herbicide as their sole carbon source. Concurrently, a bacterial community analysis explored bacterial diversity in soils treated or untreated with the herbicide S-metolachlor determining the effects on bacterial communities of continuous herbicide application. The cultivable part of the bacterial community, a collection with a prevalence of strains belonging to genera Pseudomonas, Serratia, and Brucella, exhibited diverse PGP potential, biocontrol potential, and soil quality improvement abilities. Further studies evinced that, when strains were combined into consortia and used to inoculate maize, it resulted in a positive impact on both seed germination and early-stage plant development. Root colonization dynamics and microbiome analysis indicated the successful establishment of consortia bacterial partners without any significant shift in host-maize root biodiversity. The HHCT bacterial collection holds promise for acting as a source of beneficial bacteria that promote crop yield while maintaining herbicide tolerance.