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Plant growth-promoting bacteria (PGPB) can enhance plant health by facilitating nutrient uptake, nitrogen fixation, protection from pathogens, stress tolerance and/or boosting plant productivity. The genetic determinants that drive the plant–bacteria association remain understudied. To identify genetic loci highly correlated with traits responsive to PGPB, we performed a genome-wide association study (GWAS) using an Arabidopsis thaliana population treated with Azoarcus olearius DQS-4T. Phenotypically, the 305 Arabidopsis accessions tested responded differently to bacterial treatment by improving, inhibiting, or not affecting root system or shoot traits. GWA mapping analysis identified several predicted loci associated with primary root length or root fresh weight. Two statistical analyses were performed to narrow down potential gene candidates followed by haplotype block analysis, resulting in the identification of 11 loci associated with the responsiveness of Arabidopsis root fresh weight to bacterial inoculation. Our results showed considerable variation in the ability of plants to respond to inoculation by A. olearius DQS-4T while revealing considerable complexity regarding statistically associated loci with the growth traits measured. This investigation is a promising starting point for sustainable breeding strategies for future cropping practices that may employ beneficial microbes and/or modifications of the root microbiome.