It has been reported that environmental factors, such as industrial pollution, environmental toxins, environmental hormones, and global warming contribute to the oxidative stress-induced deterioration of oocyte quality and female fertility. However, the prevention or improvement approaches have not been fully elucidated. Here, we explored the mechanism regarding how Mogroside V (MV), a main extract of Siraitia grosvenorii, improves the oxidative stress-induced meiotic defects in porcine oocytes. Our results showed that MV supplementation restores the defective oocyte maturation and cumulus cell expansion caused by H2O2 treatment. We further found that MV supplementation promoted the oocyte cytoplasmic maturation through preventing cortical granules from the aberrant distribution, and drove the nuclear maturation by maintaining the cytoskeleton structure. Notably, our single-cell RNA sequencing data indicated that H2O2-treated oocytes led to the oxidative stress primarily through two pathways ‘meiosis’ and ‘oxidative phosphorylation’. Lastly, we evaluated the effects of MV supplementation on the mitochondrial distribution pattern and membrane potential in H2O2-treated oocytes, revealing that MV supplementation eliminated the excessive ROS induced by the mitochondrial abnormalities and consequently suppressed the apoptosis. In conclusion, our study demonstrates that MV supplementation is an effective approach to ameliorate the oxidative stress-induced meiotic defects via recovering the mitochondrial integrity in porcine oocytes.