The meiotic recombination checkpoint reinforces the order of events during meiotic prophase I, ensuring the accurate distribution of chromosomes to the gametes. The AAA+ ATPase Pch2 remodels the Hop1 axial protein enabling adequate levels of Hop1-T318 phosphorylation to support the ensuing checkpoint response. While these events are localized at chromosome axes, the checkpoint activating function of Pch2 relies on its cytoplasmic population. In contrast, forced nuclear accumulation of Pch2 leads to checkpoint inactivation. Here, we reveal the mechanism by which Pch2 travels from the cell nucleus to the cytoplasm to maintain Pch2 cellular homeostasis. Leptomycin B treatment provokes the nuclear accumulation of Pch2, indicating that its nucleocytoplasmic transport is mediated by the Crm1 exportin recognizing proteins containing Nuclear Export Signals (NESs). Consistently, leptomycin B leads to checkpoint inactivation and impaired Hop1 axial localization. Pch2 nucleocytoplasmic traffic is independent of its association with Zip1 and Orc1. We also identify a functional NES in the non-catalytic N-terminal domain of Pch2 that is required for its nucleocytoplasmic trafficking and proper checkpoint activity. In sum, we unveil another layer of control of Pch2 function during meiosis involving nuclear export via the exportin pathway that is crucial to maintain the critical balance of Pch2 distribution among different cellular compartments. Author summary: Meiosis is a specialized cell division essential for sexual reproduction because it is responsible for halving the number of chromosomes during gametogenesis. Meiosis involves a series of events that culminate in the interaction between maternal and paternal chromosomes, and the exchange of genetic material by recombination. These processes not only generate genetic diversity, but also, and more important, are essential to promote proper distribution of chromosomes to the gametes. Meiotic cells possess surveillance mechanisms, called checkpoints, that reinforce the proper order of events during the meiotic cell cycle, ensuring the accurate segregation of chromosomes and preventing the formation of aneuploid gametes. The Pch2 protein is an evolutionarily-conserved ATPase that functions in the yeast meiotic recombination checkpoint. Pch2 localizes in the nucleolus, chromosomes, and the cytoplasm, performing distinct and, in some cases, opposite functions in these different subcellular compartments. In this work, we uncover the mechanism that Pch2 uses to travel from the nucleus to the cytoplasm; in particular, the Crm1 exportin pathway. We also identify and characterize a nuclear export signal in the non-catalytic domain of Pch2 required for its nucleocytoplasmic trafficking. Thus, our work contributes to understanding how the critical balance of Pch2 subcellular distribution is achieved to support faithful meiotic completion. [ABSTRACT FROM AUTHOR]