Heavy metal stress, including from chromium, has detrimental effects on crop growth and yields worldwide. Plant growth-promoting rhizobacteria (PGPR) have demonstrated great efficiency in mitigating these adverse effects. The present study investigated the potential of the PGPR strain Azospirillum brasilense EMCC1454 as a useful bio-inoculant for boosting the growth, performance and chromium stress tolerance of chickpea (Cicer arietinum L.) plants exposed to varying levels of chromium stress (0, 130 and 260 µM K2Cr2O7). The results revealed that A. brasilense EMCC1454 could tolerate chromium stress up to 260 µM and exhibited various plant growth-promoting (PGP) activities, including nitrogen fixation, phosphate solubilization, and generation of siderophore, trehalose, exopolysaccharide, ACC deaminase, indole acetic acid, and hydrolytic enzymes. Chromium stress doses induced the formation of PGP substances and antioxidants in A. brasilense EMCC1454. In addition, plant growth experiments showed that chromium stress significantly inhibited the growth, minerals acquisition, leaf relative water content, biosynthesis of photosynthetic pigments, gas exchange traits, and levels of phenolics and flavonoids of chickpea plants. Contrarily, it increased the concentrations of proline, glycine betaine, soluble sugars, proteins, oxidative stress markers, and enzymatic (CAT, APX, SOD, and POD) and non-enzymatic (ascorbic acid and glutathione) antioxidants in plants. On the other hand, A. brasilense EMCC1454 application alleviated oxidative stress markers and significantly boosted the growth traits, gas exchange characteristics, nutrient acquisition, osmolyte formation, and enzymatic and non-enzymatic antioxidants in chromium-stressed plants. Moreover, this bacterial inoculation upregulated the expression of genes related to stress tolerance (CAT, SOD, APX, CHS, DREB2A, CHI, and PAL). Overall, the current study demonstrated the effectiveness of A. brasilense EMCC1454 in enhancing plant growth and mitigating chromium toxicity impacts on chickpea plants grown under chromium stress circumstances by modulating the antioxidant machinery, photosynthesis, osmolyte production, and stress-related gene expression.