Bacterial wilt, caused by the soil-borne pathogen Ralstonia solanacearum, poses a significant threat to tomato crops worldwide. This study aims to assess the microbial potential of rhizobacterial isolates obtained from spent mushroom compost in suppressing bacterial wilt of tomatoes. Spent mushroom compost is a byproduct of mushroom cultivation and is known to harbor diverse microbial communities with potential plant-beneficial properties. Tomato leaves that were contaminated were collected from a number of places in the Rawalpindi Area, Punjab, Pakistan. Rhizobacterial isolates were collected from the rhizosphere of tomato plants grown in the presence of spent mushroom compost. These isolates were then subjected to laboratory evaluations for their antagonistic activity against R. solanacearum. Selected rhizobacterial isolates were further characterized for their plant growth-promoting traits. The potential of these isolates to enhance tomato plant growth and confer resistance against bacterial wilt was evaluated through greenhouse experiments. Results indicated that certain rhizobacterial isolates exhibited substantial antagonistic activity against R. solanacearum. Additionally, these isolates demonstrated multiple plant growth-promoting traits, suggesting a potential dual role in both pathogen suppression and plant enhancement. Greenhouse experiments revealed a significant reduction in the incidence of bacterial wilt in tomato plants and increase in the growth promotion traits were observed while treated with the selected rhizobacterial isolates alone and in combination compared to control groups. The findings from this study highlight the promising role of rhizobacterial isolates associated with spent mushroom compost in managing bacterial wilt in tomatoes.