Acinetobacter baumannii is an opportunistic nosocomial pathogen and causes bacteremia, urinary tract infections, meningitis, and pneumonia. The emergence of drug-resistant strain makes most of the current antibiotics ineffective. It is high time to screen some therapeutics against drug-resistant strains. Plant-based medicines have recently emerged as one of the important therapeutic choices. Therefore, in the present study, we have screened the metabolites of Phyllanthus emblica, Ocimum tenuiflorum, and Murraya koenigii for their antibacterial effect against carabapenem-resistant strain (RS-307) of A. baumannii. The result showed that the methanolic extract of P. emblica inhibits the growth of RS-307. The composition of this extract was determined using phytochemical screening and nuclear magnetic resonance (1D and 2D-NMR). The mechanism of action of the plant extract was validated by estimating reactive oxygen species (ROS), lipid peroxidation, protein carbonylation, and membrane damage. The result showed that treatment with this extract showed a significant elevation in the production of ROS generations, lipid peroxidation, and protein carbonylation. This confirms that plant extract treatment confirmed ROS-dependent membrane damage mechanism. The NMR result showed the presence of ethyl gallate, ellagic acid, chebulagic acid, quercetin, flavonoid, and alkaloid. To validate the antimicrobial activity of the secondary metabolite (i.e., gallic acid), we synthesized gallate-polyvinylpyrrolidone-capped hybrid silver nanoparticles (G-PVP-AgNPs) and characterized using Fourier transform infrared spectroscopy (FTIR). G-PVP-AgNPs showed good antimicrobial activity against RS-307, and its mechanism of action was investigated using fluorescence and transmission electron microscopy and FTIR that confirmed ROS-dependent killing mechanism. Therefore, the present study highlighted and recommended the use of G-PVP-AgNPs as suitable therapeutics against carbapenem-resistant A. baumannii. CI - Copyright (c) 2020 American Chemical Society.