Declining oocyte quality is the driving cause of subfertility and subsequent infertility with advanced age. We know that fertility in older females can be rescued by the use of donor oocytes from younger women, showing that they can support pregnancy, but oocyte quality is reduced. It is thought that the accumulation of oxidative stress with age damages protein and DNA within the oocyte, resulting in developmental failure. Although the oocyte contains protective mechanisms to prevent this, it is not clear what causes this to fail in individual low-quality oocytes. We hypothesise that mRNA deficiencies in aged oocytes impair the ability of the embryo to replace damaged proteins required for meiotic progression and early development. This study compares a large number of single oocyte transcriptomes from reproductive-age (3-month-old, n=31) mice and mice experiencing reproductive decline (10-month-old, n=36), where reduced litter sizes reflect impaired oocyte quality. This allowed for the identification of differentially expressed genes and changes to large regulatory networks in aged oocytes using a weighted gene network co-expression analysis. Unlike a traditional pooled analysis, we were also uniquely positioned to identify individual (potentially) low-quality oocytes. Gene ontology showed dysregulation of cytoskeletal genes crucial for processes occurring in meiosis and embryonic mitosis, consistent with the increased rates of meiotic failure with age. Aged oocytes also have impaired mRNA processing and storage genes. This suggests that translation initiation in the oocytes is dysregulated, which may cause early embryos to be deficient in proteins needed for early embryo development. Finally, there was altered expression of ubiquitination and protein degradation transcripts, which are essential for discarding oocyte-specific proteins before embryogenesis can proceed. We provide strong evidence to support emerging theories that impaired function of the proteasomal pathway and the accumulation of damaged protein underlie the age-related decline in oocyte quality.