An understanding of the biological effects of androgen actions via the androgen receptor (AR) in female reproduction has only recently begun to be unraveled. We generated global (ARKO) and granulosa cell specific (GCARKO) AR knockout female mice using Cre/LoxP recombination. ARKO females have prolonged estrous cycles (P<0.05) and are sub-fertile, with a 60% reduction in litter size (P<0.01). AR signaling is essential for optimal ovulatory function, as ARKO females have significantly reduced corpora lutea (P<0.01) and naturally ovulated oocyte numbers (P<0.01). Reciprocal ovary transplant experiments showed both intra-ovarian and extra-ovarian (neuroendocrine) defects are responsible for the ovulatory deficit in ARKO females. Neuroendocrine defects include our findings that ARKO females often exhibit a mistimed endogenous ovulatory LH surge as well as diminished pre-ovulatory serum estradiol (E2) (P<0.01) and LH (P<0.05) surge levels during late proestrus. However, this reduced LH response in ARKO females can be rescued by OVX and E2 priming or treatment with endogenous GnRH. Intra-ovarian defects are also evident as ARKO ovaries collected at proestrus (preovulatory stage) exhibit more unhealthy large antral follicles (P<0.05), and fewer preovulatory follicle (P<0.05) and corpora lutea numbers (P<0.01). Further support for an ovarian defect comes from our findings that selective loss of granulosa cell AR actions during preantral and antral stages of development leads to a 24% reduction in litters (P<0.05), a premature reduction in female fecundity with a decrease in total pups born over 6 months (P<0.05). Furthermore, follicle health was reduced in GCARKO ovaries (P<0.01) and oocyte viability diminished with a reduction in the percentage of ovulated oocytes to be fertilized after natural mating (P<0.05). These findings reveal that AR actions play an important role in maintaining normal ovarian function and female fertility by influencing neuroendocrine regulation of ovarian function, as well as, intra-ovarian control of follicle development.