Fungal phytopathogens threaten global food security by damaging crops and lowering their yields. Chemical fungicides, though effective, harm the health and the environment. Urgent action is needed to find sustainable solutions. This study aimed to use biogenic silver nanoparticles (AgNPs) fabricated using Aspergillus fumigatus as an alternative fungicide to control Fusarium wilt in tomato plants. AgNPs were spherical, 38 nm in size, -25.8 mV charge, and surrounded with functional groups, i.e., hydroxyl, amine, and carbonyl. The AgNPs (80 µg/mL) had considerable antioxidant activity, scavenging 89% of 2,2-diphenyl-1-picrylhydrazyl (DPPH) free radicals while inhibiting the growth of pathogenic fungi: Fusarium oxysporum, Fusarium solani, Rhizoctonia solani, and Alternaria solani. Also, AgNPs (80 µg/mL) enhanced the seed germination by 98%. Based on the in vivo tests, AgNPs significantly reduced the Fusarium wilt disease index caused by Fusarium solani in tomatoes by 94% while enhancing the fruit weight increases by 45% and the tomato yield by 60% in drenched AgNPs-treated plants. AgNPs significantly influenced the expression of key genes [1-aminocyclopropane-1-carboxylate (ACCO), NADPH oxidase (RBOH1), tomato lipoxygenase A (TomLoxA), chalcone synthase (CHS), and pathogenesis-related protein 1 (PR1a)] in F. solani-infected tomato plants; these genes induced the plant growth hormones secretion, phenolic compounds, flavonoids, and systemic acquired resistance (SAR). AgNPs generally upregulated defense gene transcription and enhanced plant growth and antioxidant activity. Soil drenching with AgNPs was more effective in downregulating the peroxidase (POD) and catalase (CAT) to normal levels compared to the infected control than foliar application. Compared to the infected control, the chlorophyll content increased by 200 and 160% in drench and foliar applications, while carotenoid content increased by 84 and 62%, respectively. Biogenic AgNPs fabricated by the Aspergillus fumigatus strain are recommended as a biocontrol agent against phytopathogenic fungi.