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Simple Summary: In modern aquaculture, fish have been subjected to intensive stressful conditions, which threaten their growth rate and increase their susceptibility to bacterial diseases. Innovative and sustainable production strategies in aquaculture have encouraged the utilization of plant-derived bioactive molecules (phytogenics) in fish diets, especially when they were used in a unique blend offering enumerable growth and health benefits. Therefore, our research was conducted to uncover the potential nutritional and immunological impacts of thymol (Thy) and/or thymoquinone (ThQ) with a disease shielding effect against Aeromonas sobria. Herein, the integration of dietary Thy and ThQ provided an efficient way to improve fish growth-related parameters and muscle antioxidant capacity. Moreover, we presented evidence for the unique immune-stimulating role of a Thy and ThQ combination with a successful forefront defense against A. sobria experimental infection in Nile tilapia. Our key findings motived the application of a dietary blend comprising Thy and ThQ as a functional feed that fights the challenges facing the aquaculture industry with maximized fish productivity. Plant-derived bioactive compounds with promising nutritional and therapeutic attributes (phytogenics) are among the top priorities in the aquaculture sector. Therefore, the impact of thymol (Thy) and/or thymoquinone (ThQ) on the growth, immune response antioxidant capacity, and Aeromonas sobria (A. sobria) resistance of Nile tilapia was investigated. Four fish groups were fed a control diet and three basal diets supplemented with 200 mg/kg diet of Thy or ThQ and a blend of both Thy and ThQ at a level of 200 mg/kg diet each. At the end of the feeding trial (12 weeks), the tilapias were challenged intraperitoneally with virulent A. sobria (2.5 × 108 CFU/mL) harboring aerolysin (aero) and hemolysin (hly) genes. The results revealed that tilapias fed diets fortified with a combination of Thy and ThQ displayed significantly enhanced growth rate and feed conversion ratio. Notably, the expression of the genes encoding digestive enzymes (pepsinogen, chymotrypsinogen, α-amylase and lipase) and muscle and intestinal antioxidant enzymes (glutathione peroxidase, catalase and superoxide dismutase) was significantly upregulated in Thy/ThQ-fed fish. An excessive inflammatory response was subsided more prominently in the group administrated Thy/ThQ as supported by the downregulation of il-β, il-6 and il-8 genes and in contrast, the upregulation of the anti-inflammatory il-10 gene. Remarkably, dietary inclusion of Thy/ThQ augmented the expression of autophagy-related genes, whilst it downregulated that of mtor gene improving the autophagy process. Furthermore, Thy/ThQ protective effect against A. sobria was evidenced via downregulating the expression of its aero and hly virulence genes with higher fish survival rates. Overall, the current study encouraged the inclusion of Thy/ThQ in fish diets to boost their growth rates, promote digestive and antioxidant genes expression, improve their immune responses and provide defense against A. sorbia infections with great economic benefits. [ABSTRACT FROM AUTHOR]