FZR1 is an activator of the Anaphase Promoting Complex (APC) and is an important regulator of cell cycle events including M-phase exit and the maintenance of genomic stability in somatic cells. FZR1 also plays a role in governing the timing of meiotic re-entry and MI progression in fully-grown mammalian oocytes. Using a germ cell-specific mouse knockout model of FZR1 (FZR1Δ) in which the protein is lost in embryonic life, we now identify an essential role for this protein in completion of meiosis I in both the male and female germ cells. Loss of FZR1 led to both a mitotic and meiotic defect in the male that caused complete infertility due to lack of mature spermatozoa. Spermatogonia in the prepubertal testis of these mice displayed abnormal proliferation and delayed entry into meiosis. Although early recombination events of double strand break formation and synaptonemal protein loading were initiated, male germ cells failed to progress beyond the zygotene stage and underwent catastrophic meiotic arrest and apoptosis. Nuclear levels of the APCFZR1 substrate, cyclinB1 were increased in the nuclei of FZR1Δ germ cells suggesting a defect in CDK1 kinase activity in these cells. In female FZR1Δ mice, sub-fertility was observed with loss of embryonic germs cells around the time of zygotene-pachytene transition with subsequent premature ovarian failure by 5 months of age. We conclude that FZR1 is a critical regulator of meiotic entry timing and early Prophase I progression in mammalian germ cells.