In vitro maturation (IVM) of oocytes is pivotal for successful embryo production. Cumulus cells (CCs) contribute to oocyte maturation through the secretion of hormones and nutrients, with proper autophagic activity being crucial for this process. However, the role of autophagy in CCs remains underexplored. Siraitia grosvenorii extract Mogroside III (MIII), known for its antioxidant properties, has yet to be extensively studied for its impact on bovine oocyte IVM and its potential regulatory effects on autophagy. This study assessed the influence of MIII on autophagic activity in CCs and its subsequent effects on oocyte developmental potential. The results demonstrated that MIII enhanced bovine oocyte IVM, promoted CC expansion, and supported embryonic development. Transcriptomic analysis indicated that MIII upregulated the expression of autophagy-related genes. In vitro experiments on CCs revealed that MIII increased LC3B protein levels, reduced SQSTM1 accumulation, and upregulated the gene expression of LC3, Beclin1, and ATG5. In co-culture systems, autophagy inhibition in CCs impaired oocyte IVM and embryonic development, but MIII alleviated these effects, restoring oocyte developmental capacity compromised by 3-MA-induced autophagy inhibition. Mechanistically, MIII facilitated the degradation of WT1 by upregulating LC3B, influencing CC differentiation, enhancing FSHR synthesis, and increasing estrogen and progesterone secretion. In conclusion, MIII enhances oocyte developmental potential by modulating autophagy in CCs.