Pseudomonas aeruginosa is a repertoire of several virulence factors that create a frightening high pathogenicity level as well as high antimicrobial resistance toward commercially used antibiotics. Therefore, finding a new alternative to traditional antimicrobials is a must. Resveratrol is a very famous phytochemical that harbors many beneficial health properties by possessing antibacterial, anti-inflammatory, and antioxidant properties. The current study aimed to explore the antimicrobial efficacy of resveratrol against P. aeruginosa and explore its ability to accelerate wound healing in a murine model. The obtained results revealed the potent antimicrobial, antivirulence, and wound-healing accelerating potentials of resveratrol against carbapenem-resistant P. aeruginosa (CRPA)-septic wounds. It significantly lowered the transcript levels of P. aeruginosa virulent genes toxA, pelA, and lasB. Additionally, resveratrol significantly accelerated skin wound healing by shortening the inflammatory phase and promoting re-vascularization, cell proliferation, re-epithelialization, and collagen deposition. Furthermore, it increased the immunoexpression of αSMA along with a reduction of the mRNA levels of VEGF, IL-1β, and TNF-α genes. Resveratrol has high therapeutic potential for the treatment of P. aeruginosa wound infection and is a prospective and promising candidate for this problem.