Epigenetic modifications strongly influence gene expression and are vital in maintaining long-term memory of cellular identity and function. As oocytes and sperm transmit epigenetic information to offspring, appropriate regulation of epigenetic programming within the male and female germlines is critical for normal offspring development. Oocyte epigenetic programming is highly complex, involving a range of epigenetic enzymes which establish a specific distribution of DNA methylation and histone modifications during oogenesis. Despite the importance of correctly establishing the unique epigenome of oocytes, epigenetic modifiers and their respective modifications are poorly described during oocyte growth. Polycomb Repressive Complex 2 (PRC2) is a broadly evolutionarily conserved epigenetic complex which catalyses Histone 3 Lysine 27 trimethylation (H3K27me3) in primary-secondary follicle oocytes. We investigated when several epigenetic modifiers and modifications were present within mouse growing oocytes relative to PRC2 subunits, and how they were impacted by loss of PRC2 function. We provide the first immunofluorescent profile of various epigenetic modifiers and modifications in mouse oocytes of primordial to antral follicles. Through characterisation of the spatial and temporal regulation of these epigenetic factors, we demonstrate that oocyte epigenetic programming occurs in a highly ordered manner. Histone modification establishment and remodelling by histone methyltransferases and demethylases occurs in early oocyte growth, preceding de novo DNA methylation in secondary to antral follicle oocytes. We also show that H3K27me3 depletion within growing oocytes significantly increased nuclear levels of H3K36me3 methyltransferase, SETD2, in early-mid oocyte growth, which may region-specifically reorganise H3K36me3. Our results provide valuable insights into maternal epigenetic programming as well as PRC2 function in oocytes. This work is important in understanding how a distinctive arrangement of epigenetic modifications is carefully established during oocyte growth. Enhanced understanding of oocyte epigenetic programming is essential as changes to the oocyte epigenome can disrupt epigenetic memory and alter offspring developmental outcomes.