The biosynthesis of nanoparticles using green technology is emerging as a cost-efficient, eco-friendly and risk-free strategy in nanotechnology. Recently, tellurium nanoparticles (TeNPs) have attracted growing attention due to their unique properties in biomedicine, electronics, and other industrial applications. The current investigation addresses the green synthesis of TeNPs using a newly isolated mangrove-associated bacterium, Gayadomonas sp. TNPM15, and their impact on the phytopathogenic fungi Fusarium oxysporum and Alternaria alternata. The biogenic TeNPs were characterized using transmission electron microscopy (TEM), scanning electron microscopy (SEM), energy-dispersive X-ray spectroscopy (EDX), X-ray diffraction (XRD), Raman spectroscopy and Fourier transform infrared (FTIR). The results of TEM revealed the intracellular biosynthesis of rod-shaped nanostructures with a diameter range from 15 to 23 nm and different lengths reaching up to 243 nm. Furthermore, the successful formation of tellurium nanorods was verified by SEM-EDX, and the XRD pattern revealed their crystallinity. In addition, the FTIR spectrum provided evidence for the presence of proteinaceous capping agents. The bioinspired TeNPs exhibited obvious inhibitory effect on the spores of both investigated phytopathogens accomplished with prominent ultrastructure alternations, as evidenced by TEM observations. The biogenic TeNPs impeded spore germination of F. oxysporum and A. alternata completely at 48.1 and 27.6 µg/mL, respectively. Furthermore, an increase in DNA and protein leakage was observed upon exposure of fungal spores to the biogenic TeNPs, indicating the disruption of membrane permeability and integrity. Besides their potent influence on fungal spores, the biogenic TeNPs demonstrated remarkable inhibitory effects on the production of various plant cell wall-degrading enzymes. Moreover, the cytotoxicity investigations revealed the biocompatibility of the as-prepared biogenic TeNPs and their low toxicity against the human skin fibroblast (HSF) cell line. The biogenic TeNPs showed no significant cytotoxic effect towards HSF cells at concentrations up to 80 μg/mL, with a half-maximal inhibitory concentration (IC50) value of 125 μg/mL. The present work spotlights the antifungal potential of the biogenic TeNPs produced by marine bacterium against phytopathogenic fungi as a promising candidate to combat fungal infections.