The contamination of soils with cadmium (Cd) threatens agricultural productivity worldwide. The ability of plants to withstand challenging circumstances is primarily contingent upon their inherent capacity for tolerance and defense. The purpose of the current work is to gain a better understanding of how the mitochondrial ATP synthase enzyme, the antioxidant defense system, redox homeostasis, and chlorophyll metabolism in tomato seedlings are regulated by nitric oxide and hydrogen sulfide under Cd stress. The results demonstrate that exposure of tomato seedlings to Cd stress resulted in a substantial decrease in the activity of ATP synthase. The plants exposed to Cd stress, exhibited an increase in chlorophyllase activity and a substantial decrease in the activity of δ-aminolevulinic acid dehydratase, which resulted in a substantial loss of chlorophyll content. Elevation in the antioxidant defense system under Cd stress could not bring a significant positive change in the plants’ defense system that resulted in lipid peroxidation and leakage of electrolytes. Incubation of Cd-stressed seedlings with nitric oxide donor S-nitrosoglutathione (GSNO) proved remarkable in improving the performance of the plants. The results exhibit that GSNO application improved the activity of ATP synthase, superoxide dismutase, peroxidase, and catalase and the performance of the ascorbate-glutathione system, which efficiently scavenged excess reactive oxygen species. The positive effect of GSNO application was also shown by decreased lipid peroxidation and electrolyte leakage. However, application of DL-propargylglycine (a biosynthesis inhibitor of hydrogen sulfide) to the stressed-seedlings reversed the effect of GSNO, which resulted in the weak performance of the defense system and the commencement of oxidative stress. The results of the study substantiate that nitric oxide, in association with endogenous hydrogen sulfide, was remarkable in providing protection to the plants against Cd toxicity.