Hydrogen sulfide (H2S) has emerged as an important signaling molecule and plays a significant role during different environmental stresses in plants. The present work was carried out to explore the potential role of H2S in reversal of dehydration stress-inhibited O-acetylserine (thiol) lyase (OAS-TL), l-cysteine desulfhydrase (LCD), and d-cysteine desulfhydrase (DCD) response in arugula (Eruca sativa Mill.) plants. Dehydration-stressed plants exhibited reduced water status and increased levels of hydrogen peroxide (H2O2) and superoxide (O2•−) content that increased membrane permeability and lipid peroxidation, and caused a reduction in chlorophyll content. However, H2S donor sodium hydrosulfide (NaHS), at the rate of 2 mM, substantially reduced oxidative stress (lower H2O2 and O2•−) by upregulating activities of antioxidant enzymes (superoxide dismutase, peroxidase, and catalase) and increasing accumulation of osmolytes viz. proline and glycine betaine (GB). All these, together, resulted in reduced membrane permeability, lipid peroxidation, water loss, and improved hydration level of plants. The beneficial role of H2S in the tolerance of plants to dehydration stress was traced with H2S-mediated activation of carbonic anhydrase activity and enzyme involved in the biosynthesis of cysteine (Cys), such as OAS-TL. H2S-treated plants showed maximum Cys content. The exogenous application of H2S also induced the activity of LCD and DCD enzymes that assisted the plants to synthesize more H2S from accumulated Cys. Therefore, an adequate concentration of H2S was maintained, that improved the efficiency of plants to mitigate dehydration stress-induced alterations. The central role of H2S in the reversal of dehydration stress-induced damage was evident with the use of the H2S scavenger, hypotaurine.