The genetic background of many female reproductive health diagnoses remains uncharacterized, compromising our understanding of the underlying biology. Here, we map the genetic architecture across 42 female-specific health conditions using data from up to 293,618 women from two large population-based cohorts, the Estonian Biobank and the FinnGen study. Our study illustrates the utility of genetic analyses in understanding women's health better. As specific examples, we describe genetic risk factors for ovarian cysts that elucidate the genetic determinants of folliculogenesis and, by leveraging population-specific variants, uncover new candidate genes for uterine fibroids. We find that most female reproductive health diagnoses have a heritable component, with varying degrees of polygenicity and discoverability. Finally, we identify pleiotropic loci and genes that function in genital tract development (WNT4, PAX8, WT1, SALL1), hormonal regulation (FSHB, GREB1, BMPR1B, SYNE1/ESR1) and folliculogenesis (CHEK2), underlining their integral roles in female reproductive health.