In mammalian meiotic prophase I, hundreds of double-strand breaks are induced throughout the genome, but only a subset are repaired as crossovers. Crossovers ensure proper chromosomal segregation at the first meiotic division. Errors in crossover segregation can lead to aneuploid gametes. Oocytes exhibit a high rate of chromosomal abnormalities, and these abnormalities can be traced back to defects in crossover formation. Thus, highlighting the need to understand sex-specific differences in crossover regulation. Cyclin N-terminal domain containing-1 (CNTD1) is a key regulator of crossover formation with putative sex-specific roles. In spermatocytes, CNTD1 functions in a cyclin-independent manner, designating crossover sites through interactions with Replication Factor C and promoting cell cycle progression via the SKP1-CUL1-F-box E3 ubiquitin ligase complex. While CNTD1 in oocytes is present at the same molecular weight as in spermatocytes, Cntd1-/- oocytes exhibit extensive synapsis defects not observed in spermatocytes. These defects result in ovarian reserve depletion without altering ovarian morphology, distinguishing them from other prophase I mutants. This underscores a sex-specific role for CNTD1 in crossover designation and synapsis, essential for oocyte quality and ovarian reserve maintenance through checkpoint-mediated error surveillance. CNTD1 functions by interacting with core subunits of Replication Factor C (RFC) complexes, which are crucial for DNA replication, repair, and sister chromatid cohesion in somatic cells. Conditional ablation of Replication Factor C subunit 3 (Rfc3) maintains fertility but leads to reduced testis mass and sperm counts. While most Rfc3cKO spermatocytes exhibit normal morphology, a subset displays synapsis defects reminiscent of early prophase I mutants. Though current genetic tools do not completely abrogate Rfc3, these findings provide a foundation for further investigation into RFC-like complexes and their roles in crossover regulation. This work examines the sexually dimorphic regulation of crossovers, from double-strand break formation to crossover site selection. By analyzing how defects in CNTD1 and RFC-like complexes contribute to aneuploidy, these findings provide critical insights into the mechanisms ensuring meiotic fidelity and genome stability.