Cucumber wilt, caused by Fusarium oxysporum f. sp. cucumerinum (FOC), is a soilborne disease that poses a significant threat to cucumber production, resulting in substantial yield losses. This study aimed to evaluate the biocontrol and growth-promoting effects of Bacillus velezensis, a highly active bacterial strain. In vitro assays revealed that B. velezensis F9 exhibited broad-spectrum antifungal activity against eight plant pathogenic fungi, with inhibition ratio ranging from 62.66% to 88.18%. Additionally, the strain displayed the ability to produce IAA (5.97 ± 1.75 µg/mL), fix nitrogen, produce siderophores, and form biofilms. In vitro growth promotion assays demonstrated that different concentrations of B. velezensis F9 significantly promoted cucumber seedling growth. Furthermore, two pot experiments revealed that the strain exhibited biocontrol efficacy against cucumber wilt, with disease control rates ranging from 42.86% to 67.78%. Notably, the strain significantly increased the plant height, fresh weight, and dry weight, with increases ranging from 20.67% to 60.04%, 40.27% to 75.51%, and 22.07% to 52.54%, respectively. Two field trials confirmed the efficacy of B. velezensis F9 in controlling cucumber wilt, with disease control rates of 44.95% and 33.99%, respectively. The strain effectively alleviated the dwarfing and wilting symptoms caused by the pathogen. Compared with the FOC treatment, the F9 + FOC treatment significantly increased the plant height, fresh weight, and dry weight, with increases of 43.85% and 56.28%, 49.49% and 23.70%, and 36.25% and 73.63%, respectively. Enzyme activity assays indicated that inoculation significantly increased SOD activity in cucumber leaves and neutral phosphatase, sucrase, and urease activity in rhizosphere soil. Correlation analysis revealed a negative correlation between the disease index and plant height, fresh weight, dry weight, and peroxidase activity, with correlation coefficients of -0.53, -0.60, -0.38, and -0.45, respectively. These findings suggest that plant height, fresh weight, and dry weight are significantly negatively correlated with the cucumber disease index, highlighting their importance as indicators for evaluating the biocontrol efficacy of B. velezensis F9. In conclusion, B. velezensis F9 is a highly effective plant growth-promoting rhizobacterium with excellent biocontrol potential, showcasing promising applications in agricultural production.