Age-associated declines in female fertility evident after only 30 years of age involve a decrease in total follicle number and oocyte quality. In addition, physiologic age-related changes include increased fibrosis, expanded stromal cell compartment, and changed ovarian medullary and cortex volume. The molecular mechanisms driving age-associated female fertility decline remain unclear. Because of the heterogeneous nature of ovarian cells, cell type-specific changes in gene expression have historically been difficult to ascertain. Single-cell tagged reverse transcription (STRT) enables high-throughput single-cell RNA sequencing (scRNA-seq) with detection of abundant genes per cell. This study aimed to survey the first comprehensive single-cell transcriptomic landscape of ovarian aging using cynomolgus monkey models. Ovaries were obtained from 4 juvenile (4-5 years) and 4 aged (18-20 years) cynomolgus monkeys. The genus Macaca undergo menopause at 25 years, so the aged monkeys were premenopausal. Gene-expression signatures were obtained for 7 ovarian cell types and 4 oocyte subtypes (C1-C4) during folliculogenesis by scRNA-seq using the modified STRT technique. To compare genomic alterations observed to those in humans, human granulosa cells (hGCs) were obtained from healthy women aged 21 to 46 years and similarly analyzed. A total of 2601 cells with high-quality transcriptomes were obtained using scRNA-seq (418 oocytes, 2183 somatic cells). Age-associated changes to the ovarian gene-expression pattern indicated oxidative damage is an essential factor in ovarian aging. Calculation of age-relevant coefficient of variation indicated that aging resulted in higher variability in oocytes from early-stage follicles than those from late-stage follicles. Gene ontology analysis revealed several genes involved in oxidative phosphorylation and oxidoreductase activity including GPX1 and GSR to be downregulated in oocyte subtype C2 among the aged primates. This appears to be a unique aging feature of early-stage oocytes and may contribute to the increased oxidative damage incurred during ovarian aging. Among the aged primate granulosa cells, gene ontology analysis revealed genes involved in positive regulation of apoptosis were upregulated, whereas genes involved in oxidoreductase activity, including IDH1, PRDX4, and NDUFB10, were downregulated. Increased DNA oxidation, damage, and apoptosis were observed in aged monkey GCs. Aging-associated increases in reactive oxidation species and apoptosis were observed in the hGCs, supporting the notion of increased oxidative stress being linked to ovarian aging. Aging-associated downregulation of IDH1, PRDX4, and NDUFB10 was observed in the hGCs. This comprehensive single-cell transcriptomic analysis revealed several insights into the cell type-specific gene signatures of the primate ovary. The results of this study indicate that IDH1 and NDUFB10 protect GCs from aging-related oxidative stress in both humans and monkeys and suggest upregulation of oxidative damage markers and downregulation of antioxidant proteins as potential mechanisms for primate ovarian aging.