In the mammalian ovary, the proper assembly, activation and quiescence of follicles is crucial for oocyte survival and reproduction, and depends on the concerted activities of multiple signalling pathways, including WNT. The Pro(renin) Receptor (PRR), encoded by the X-linked Atp6ap2 gene, is best known for its role in the renin-angiotensin system. However recently, its importance as a mediator of canonical WNT signalling has emerged based on its function as a bridge between the WNT receptor LRP6 and the vacuolar H+-ATPase (V-ATPase). These findings, together with our observation that Atp6ap2 is highly expressed in the developing gonads, led to our hypothesis that PRR is important for ovarian development. To investigate the function of PRR in the developing ovary, we generated ovarian somatic cell-specific Atp6ap2 conditional knockout mice. Here, we present the ovarian phenotype of these mice and show that PRR is essential for folliculogenesis and oocyte survival, and is linked to diverse cellular mechanisms in the ovary including cell differentiation, cell polarity, gap/adherens junction formation and autophagy. Our findings therefore suggest PRR plays a pleiotropic role in the developing mammalian ovary.