The Piwi-interacting RNA (piRNA) pathway is an RNA silencing pathway that represses the expression of transposable elements (TE) in spermatogonia via binding of piRNAs to their complimentary RNA targets. Mammalian piRNAs are 26-31 nt in length and are 2’-O-methylated at their 3’ termini. The role of piRNAs in adult male germ cells types, however, wherein the majority of piRNA sequences are not complementary to TE sequences, remains poorly defined. To address this question, and the role of piRNAs in female fertility, we have used a unique mouse model of HENMT1 dysfunction (Henmt1Pin/Pin). HENMT1 is an RNA methyltransferase that acts to add stabilizing 3’ methyl groups to piRNAs. The loss of piRNAs in adult male germ cells results in male sterility characterized by TE over-expression, the precocious expression of haploid germ cell transcripts in meiotic cells and a catastrophic deregulation of the haploid germ cell program. Our data strongly suggests a role for piRNA in promoting a heterochromatic state in the regulatory regions of many spermiogenesis genes during meiosis and their necessity to set an appropriate gene expression program. Further our data show Henmt1 dysfunction in female mice leads to a sub-fertility phenotype reminiscent of premature ovarian failure in humans. Specifically, Henmt1Pin/Pin females are fertile while young, but have depleted ovarian reserves by six months-of-age. Further, even when young the quality of oocytes from Henmt1Pin/Pin females is significantly compromised. Collectively these data support a role for HENMT1 and piRNAs in oocyte survival during the perinatal period and in the regulation genes critically involved in adult oocytes function.