This work aimed at elucidating the role of bacteria present in the gut of the earthworm Metaphire posthuma in plant growth promotion and toxic trace elements (TTEs) bioremediation. We isolated and identified three bacterial strains Bacillus safensis (MF 589718), Bacillus flexus (MF 589717) and Staphylococcus haemolyticus (MF 589719) among which the Bacillus strains appeared to be significantly more potent than the Staphylococcus strain (P < 0.05) in promoting plant growth and removing TTE (Cr(VI), Cu(II) and Zn(II)) from aqueous media. These strains exhibited several plant growth promoting traits (e.g., indole acetic acid (IAA), gibberellic acid (GA) and ammonium ion production, 1-aminocyclopropane- 1-carboxylic acid (ACC) deaminase activity, and phosphate solubilizing potential). In a pot trial, the gut isolates improved Vigna radiata seed germination, and enhanced the leaf area (30-79%), total chlorophyll content (26-67%) and overall root-shoot biomass (32-83%) as compared to the control. Bacillus safensis and Bacillus flexus were equipotent in removing Cr(VI) (40.5 and 40.3%) from aqueous media; the former triumphed for Zn(II) removal (52.8%), while the latter performed better for Cu(II) removal (43.5%). The gut isolates successfully solubilized phosphate even in TTE-contaminated conditions. The results demonstrate that the earthworm's enteric bacteria possess inherent plant growth promoting, TTE resistance and phosphate solubilization (even under TTE stress) properties which can be further explored for their application in sustainable crop production and environmental management.