Heavy metals are toxic environmental contaminants, which severely affect microbial composition and functions and, concurrently, crop production. Due to these issues, the present study focussed on the selection of metal tolerant microbes endowed with metal detoxification abilities and their role in the management and remediation of metal contaminated soils. The metal tolerant bacterium BM2, identified as Bacillus subtilis by 16SrRNA gene sequencing, survived well under metal pressure and tolerated 1600 and 2000 μg mL−1 of Ni and Pb, respectively. The inhibitory impact of metals on wheat increased consistently with a progressive increase in metal concentration. Deposition of Ni and Pb within root and leaf and oxidative stress were validated by SEM, EDX and CLSM. The overall growth parameters of wheat grown under metal stress were improved following B. subtilis BM2 colonization. As an example, B. subtilis with 195 mg Pb kg−1 enhanced the length and dry biomass of shoots by 14% and 23%, respectively, over the control. Also, strain BM2 improved the grain yield significantly by 49% at 870 mg Ni kg−1 and by 50% at 585 mg Pb kg−1 compared to uninoculated plants. Moreover, B. subtilis BM2 relieved the metal stress on wheat and caused a significant drop in proline and malondialdehyde content and the activities of antioxidant enzymes, like catalase (CAT), superoxide dismutase (SOD) and glutathione reductase (GR). This study, therefore, provided solutions to the metal toxicity problems faced by winter wheat and clearly suggests that the metal detoxification potential of B. subtilis BM2 could be greatly useful in the management of metal polluted soils.