The role of classical genomic androgen receptor (AR) mediated actions in female reproductive physiology remain unclear. Female mice homozygous for an in-frame deletion of exon 3 of the Ar (AR^-/-) were sub-fertile, exhibiting delayed production of their first litter (AR^+/+ = 22 days vs AR^-/- = 61days, P<0.05) and producing 60% fewer pups/litter (AR^+/+: 8.1 ± 0.4 vs AR^-/-: 3.2 ± 0.9, P<0.01). Heterozygous females (AR^+/-) exhibited an age-dependent 55% (P<0.01) reduction in pups/litter, evident from 6 months of age (P<0.05) compared to AR^+/+, indicating a significant gene dosage effect on female fertility. Ovulation was defective with a significant reduction in corpora lutea numbers (48-79%, P<0.01) in 10-12 and 26 week old AR^+/- and AR^-/- females, and a 57% reduction in oocytes recovered from naturally mated AR^-/- females (AR^+/+: 9.8 ± 1.0 vs AR^-/-: 4.2 ± 1.2, P<0.01) however, early embryo development to the 2-cell stage was unaltered. The delay in 1^st litter, reduction in natural ovulation rate and aromatase expression in AR^+/- and AR^-/- ovaries, coupled with the restored ovulation rate by gonadotropin hyperstimulation in AR^-/- females, suggests aberrant gonadotropin regulation. A 2.7-fold increase (AR^+/+: 35.4 ± 13.4 vs AR^-/-: 93.9 ± 6.1, P<0.01) in morphologically unhealthy antral follicles demonstrated deficiencies in late follicular development, although growing follicle populations and growth rates were unaltered. This novel model reveals that classical genomic AR action is critical for normal ovarian function although not for follicle depletion and that haploinsufficiency for an inactivated AR may contribute to a premature reduction in female fecundity.