Post-ovulatory oocyte ageing in fish is associated with limited fertilization rate, poor embryo development, larval malformation, ploidy anomalies and various other offspring abnormalities. Many studies have focused on morphological, physiological, biochemical and histological changes that occur during oocyte ageing. However, little is known about molecular changes associated with this process. This review covers the cellular and molecular characteristics of ageing oocytes with special focus on age-associated changes affected by oxidative damage. The contribution of oxidative stress and mitochondrial dysfunction, as well as new insights into oocyte ageing in higher vertebrates, is discussed to provide direction for future studies. Investigating the genomics and proteomics of oocyte ageing, including underlying molecular mechanisms, could contribute valuable information on determinants of egg quality. Such knowledge can be translated into practical applications in aquaculture, such as supplementation of oocyte culture media with antioxidants and other agents as a means to inhibit or delay development of the aged oocyte phenotype. Identification of cellular and molecular markers associated with the oocyte ageing process will benefit such developments.