The rice zinc finger protein ZFP36 serves as a pivotal regulator of the hydrogen peroxide (HO) signaling pathway in response to abscisic acid (ABA). Its role is crucial for integrating HO signals with the plant defense mechanisms against water deficit and oxidative stress. However, it remains unclear whether ZFP36 directly modulates ABA-induced HO signaling. This study explored the effects of oxidative post-translational modifications (OxiPTMs) on ZFP36 in rice, with an emphasis on the HO-induced oxidation through its cysteine (Cys) residues. We found that ZFP36 undergoes oxidative modification as a target of HO in the presence of ABA, specifically at Cys32. Employing quantitative detection and fluorescence assays, we observed that ZFP36 oxidation enhances the expression and activity of genes encoding protective antioxidant enzymes. Moreover, our investigation into the thioredoxin (Trx) and glutaredoxin (Grx) families revealed that OsTrxh1 facilitates the reduction of oxidized ZFP36. Genetic evidence indicates that ZFP36 positively influences rice resilience to oxidative and water stress, while OsTrxh1 exerts an opposing effect. These insights reveal a distinctive pathway for plant cells to perceive ABA-induced HO signaling, advance our comprehension of HO signaling dynamics, and ABA-related plant responses, and lay a vital groundwork for enhancing crop stress tolerance.