Butylparaben (BP) is widely used in food, beverage containers, personal care products, and cosmetics, resulting in high human exposure. Previous studies reported a potential link between BP and adverse effects on human health, but its effects on female reproduction and the underlying mechanisms remain to be fully elucidated. This study examined the molecular mechanisms of BP-induced female reproductive damage and a potential therapeutic strategy. BP exposure was found to impair cumulus cell expansion, oocyte nuclear maturation, and subsequent embryonic development. BP-exposed oocytes exhibited abnormalities in microtubule structure, stability, and actin-mediated cytoskeleton dynamics. BP exposure also induced cytoplasmic maturation defects by disrupting mitochondria, the endoplasmic reticulum, and lipid metabolism. In addition, BP exposure induces oxidative stress, which interferes with DNA double-strand break repair, causes DNA damage, and ultimately leads to cell death. However, melatonin (MLT) supplementation ameliorated BP-induced meiotic and developmental defects in porcine oocytes. These results suggest that MLT plays a protective role in BP-exposed oocytes by preventing meiotic failure due to impaired nuclear and cytoplasmic maturation. MLT supplementation, therefore, offers a strategy to improve oocyte quality, fertility, and subsequent embryonic development. Our findings regarding the toxicological effects of endocrine disruptors on female reproduction suggest a novel approach for preserving female fertility.