Sustainable food production to feed nine to 10 billion people by 2050 is one of the greatest challenges we face in the 21st century. Due to anthropogenic activities, cadmium (Cd) contamination is ubiquitous with deleterious effects on plant and soil microbiota. In the current study, the phytoremediation potential of Sesbania sesban L. was investigated in Cd-spiked soil inoculated with Bacillus anthracis PM21. The Cd-spiked soil drastically reduced important plant attributes; however, inoculation of B. anthracis PM21 significantly (p ≤ 0.05) enhanced root length (17.21%), shoot length (15.35%), fresh weight (37.02%), dry weight (28.37%), chlorophyll a (52.79%), chlorophyll b (48.38%), and total chlorophyll contents (17.65%) at the Cd stress level of 200 mg/kg as compared to the respective control. In addition, bacterial inoculation improved superoxide dismutase (11.98%), peroxidase (12.16%), catalase (25.26%), and relative water content (16.66%) whereas it reduced proline content (16.37%), malondialdehyde content (12.67%), and electrolyte leakage (12.5%). Inoculated plants showed significantly (p ≤ 0.05) higher Cd concentration in the S. sesban root (118.6 mg/kg) and shoot (73.4 mg/kg) with a translocation (0.61) and bioconcentration factor (0.36), at 200 mg/kg Cd. Surface characterization of bacteria through Fourier transform infrared spectroscopy (FTIR) and scanning electron microscopy (SEM) predicted the involvement of various functional groups and cell surface morphology in the adsorption of Cd ions. Amplification of the CzcD gene in strain PM21, improved antioxidant activities, and the membrane stability of inoculated S. sesban plants conferred Cd tolerance of strain PM21. In addition, the evaluated bacterial strain B. anthracis PM21 revealed significant plant growth-promoting potential in S. sesban; thus, it can be an effective candidate for phyto-remediation of Cd-polluted soil.