Androgen actions mediated via the androgen receptor (AR) are well established as playing a vital role in male reproductive development and function, but the biological role of androgen actions in female reproduction has only recently started to be unravelled. Deciphering the specific mechanisms by which AR-mediated actions impact on ovarian function has been hindered by ambiguity of pharmacological investigations relying on aromatizable androgens that also act via estrogen receptors. Using novel global and cell-specific female AR knockout mouse models (ARKO) we confirmed a role for AR-mediated androgen actions in regulating ovarian function and maintaining optimal female fertility. Furthermore, observational human studies and animal experiments provide substantial evidence of a role for AR-mediated androgen actions in the origins of the most frequent endocrine condition in women, polycystic ovarian syndrome (PCOS). Hyperandrogenism is the most consistent PCOS characteristic, however it is unclear if androgen excess, is a cause or a consequence of PCOS. We combined a hyperandrogenised PCOS mouse model with global and cell-specific AR ARKO mice to uncover the sites of androgen action that mediate the development of the PCOS phenotype. These studies proved that global loss of AR actions (ARKO) protects females from the induction of PCOS features. Furthermore our findings highlighted the importance of non-ovarian (neuroendocrine) AR-mediated androgen actions in the origins of PCOS, as a neuron-specific loss of AR signaling protected against the development of most PCOS traits. In concert, these findings illuminate the key roles of AR-mediated androgen actions in optimizing ovarian function and female fertility, as well as providing evidence to support excess androgen receptor (AR)-mediated actions in the brain, as major drivers of the mechanisms underpinning the development of PCOS.