<p>In this study, we focused on <i>Burkholderia</i> sp. ZF6, a promising plant growth-promoting bacterium (PGPB) known for its robust heavy metal tolerance, enduring 5 mM cadmium (Cd) and 50 mM zinc (Zn), and carrying the tolerance genes <i>cad</i>A and <i>znt</i>A. ZF6 showed outstanding plant growth-promoting (PGP) abilities, including nitrogen fixation (OD₆₃₀ = 0.331 ± 0.012), over 50% DPPH radical scavenging activity, high levels of indole-3-acetic acid (IAA) production, phosphatase activity, and siderophore production. For the experimental trials, ZF6 was used to inoculate Indian mustard (<i>Brassica juncea</i>) seeds in multi-metal-contaminated soil (smelter soil), resulting in a 1.4-fold increase in seed germination. Subsequent pot experiments with soil co-contaminated with 100&#xa0;mg Cd·kg^− 1 and 2,000&#xa0;mg Zn·kg^− 1 demonstrated a 1.5- and 1.6-fold increase in shoot and root lengths, respectively, a 2.1-fold boost in vigor index, and a 1.1- to 1.2-fold rise in plant biomass. Over the experiment period, the relative abundance of <i>cad</i>A and <i>znt</i>A genes increased by 1.6- and 18.4-fold, respectively. These findings demonstrate the potential of <i>Burkholderia</i> sp. ZF6 as a biofertilizer that enhances heavy metal tolerance and promotes Indian mustard growth in highly contaminated soil while improving overall soil PGP activity.</p>