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It is essential to develop and discover alternative eco-friendly antibacterial agents due to the emergence of multi-drug-resistant microorganisms. In this study, we isolated and characterized a novel bacterium named <i>Terrabacter humi</i> MAHUQ-38^T, utilized for the eco-friendly synthesis of silver nanoparticles (AgNPs) and the synthesized AgNPs were used to control multi-drug-resistant microorganisms. The novel strain was Gram stain positive, strictly aerobic, milky white colored, rod shaped and non-motile. The optimal growth temperature, pH and NaCl concentration were 30 °C, 6.5 and 0%, respectively. Based on 16S rRNA gene sequence, strain MAHUQ-38^T belongs to the genus <i>Terrabacter</i> and is most closely related to several <i>Terrabacter</i> type strains (98.2%–98.8%). <i>Terrabacter humi</i> MAHUQ-38^T had a genome of 5,156,829 bp long (19 contigs) with 4555 protein-coding genes, 48 tRNA and 5 rRNA genes. The culture supernatant of strain MAHUQ-38^T was used for the eco-friendly and facile synthesis of AgNPs. The transmission electron microscopy (TEM) image showed the spherical shape of AgNPs with a size of 6 to 24 nm, and the Fourier transform infrared (FTIR) analysis revealed the functional groups responsible for the synthesis of AgNPs. The synthesized AgNPs exhibited strong anti-bacterial activity against multi-drug-resistant pathogens, <i>Escherichia coli</i> and <i>Pseudomonas aeruginosa</i>. Minimal inhibitory/bactericidal concentrations against <i>E. coli</i> and <i>P. aeruginosa</i> were 6.25/50 and 12.5/50 μg/mL, respectively. The AgNPs altered the cell morphology and damaged the cell membrane of pathogens. This study encourages the use of <i>Terrabacter humi</i> for the ecofriendly synthesis of AgNPs to control multi-drug-resistant microorganisms.