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We aimed to synthesize zinc oxide nanoparticles (ZnO NPs) using the endophytic fungal extract of <i>Aspergillus niger</i>. The prepared ZnO NPs were characterized, and their in vitro and in vivo antibacterial activity was investigated. Isolated endophytic fungus identification was carried out using 18S rRNA. <i>A. niger</i> endophytic fungal extract was employed for the green synthesis of ZnO NPs. The in vitro antibacterial activity of the prepared ZnO NPs was elucidated against <i>Staphylococcus aureus</i> using the broth microdilution method and quantitative real-time polymerase chain reaction (qRT-PCR). Additionally, the in vivo antibacterial activity was elucidated using a systemic infection model in mice. The biosynthesized ZnO NPs showed a maximum optical density at 380 nm with characteristic peaks on the Fourier-transform infrared spectrum. The X-ray diffraction pattern was highly matched with a standard platform of zinc oxide crystals. Energy-dispersive X-ray analysis confirmed that the main composition of nanoparticles was zinc and oxygen atoms. Scanning and transmission electron microscopies showed spherical geometry with a smooth surface. Zeta potential measurements (26.6 ± 0.56 mV) verified the adequate stability of ZnO NPs. Minimum inhibitory concentrations of ZnO NPs against <i>S. aureus</i> isolates ranged from 8 to 128 µg/mL. Additionally, ZnO NPs revealed antibiofilm activity, resulting in the downregulation of the tested biofilm genes in 29.17% of <i>S. aureus</i> isolates. Regarding the in vivo experiment, ZnO NPs reduced congestion and fibrosis in liver and spleen tissues. They also improved liver function, increased the survival rate, and significantly decreased inflammatory markers (<i>p</i> < 0.05). ZnO NPs synthesized by <i>A. niger</i> endophytic fungus revealed a promising in vivo and in vitro antibacterial action against <i>S. aureus</i> isolates.