Introduction: In recent years, the widespread environmental presence of microplastics (MPs) has raised major concerns regarding animal and human health, including potential risks to reproductive function and offspring. Methods: This study aimed to evaluate the effects of increasing concentrations of polystyrene MPs (PS-MPs; 0, 5, 50, or 100 μg/mL) on ovine cumulus-oocyte complexes (COCs) during Results: As regards CCs, increased PS-MPs uptake was highlighted at the highest exposure concentration (100 μg/mL), whereas no significant differences were observed in oocyte intracellular fluorescence intensity, compared to the control. The bioaccumulation increment in CCs monolayers was already visible after 6 h, both at 5 and 100 μg/mL, and confirmed at 24 h. The real-time PCR analysis in CCs revealed significant reductions in the expression levels of genes involved in antioxidant defense and alterations in those implicated in apoptosis. Finally, the TUNEL assay revealed a dose-dependent increase in CCs apoptotic index. Consequently, PS-MPs exposure impaired oocyte meiosis resumption by significantly reducing the maturation rates, particularly at 50 and 100 μg/mL, whereas no effects were observed at 5 μg/mL. Oocyte intracellular reactive oxygen species levels were significantly increased at all concentrations, whereas no differences in mitochondrial membrane potential were detected. The percentages of oocytes with abnormal configurations of meiotic spindle and cortical F-actin were found to be significantly increased, regardless of concentration. Finally, the cleavage rate was significantly reduced in oocytes exposed to 50 μg/mL, whereas no differences were found in the blastocyst rate at both 50 and 5 μg/mL. Discussion: In conclusion,