In vertebrates, the core mechanisms that control gametogenesis are largely multiple, complex, successive, and orchestrated by intrinsic and extrinsic factors. However, age, health status, and hormonal activity are important factors for good fertility; other intangible intracellular molecular mechanisms that manage oocyte development are still unclear Acclimatized females were randomly divided into three experimental groups (n = 60/group), each in triplicate (20 fish) in separate tanks. The first group was used as the control group (receiving no treatment), the second group, termed the T1 group, was exposed to 1/5th of the estimated LC50 of ZnO-NPs (0.69 mg/L) in water daily for two weeks (15 days), while the third group termed the T2 group was exposed to 1/5th of the estimated LC50 of ZnO-NPs daily for one month (30 days). The present study was designed toelucidate the ultrastructure changes in the ovary in response to its exposure to zinc oxide nanoparticles (ZnO-NPs) and to explore the role of autophagy and apoptosis during egg maturation and ovulation on the fertility of female zebrafish. In our study, ZnO-NPs could induce cytotoxicity in the maturing oocyte by activating autophagy and apoptosis in a caspase-dependent manner and could induce oxidative stress by generating reactive oxygen species (ROS) that elevated the mutated ovarian tP53 protein. Simultaneously, necroptosis developed, mimicking the features of apoptosis and necrosis. Collectively, ZnO-NPs created a suitable necrotic environment that led to follicular developmental retardation that altered oocyte ovulation and reduced fecundity of female zebrafish. In conclusion, our results revealed that ZnO-NPs can impair the fertility of female zebrafish in a time-dependent manner. Exposing zebrafish to 1/5th of the estimated LC50 of ZnO-NPs (0.69 mg/L) daily for one month caused cytotoxicity in the maturing oocyte by activating autophagy and apoptosis in a caspase-dependent manner and induced oxidative stress by generating ROS that elevated the mutated ovarian tP53 protein. These effects could be implicated in delaying the development of embryos and inducing embryonic abnormalities.