Significance Meiotic crossovers are essential for the production of gametes with balanced chromosome content. MutLγ (Mlh1–Mlh3) endonuclease, a mismatch repair heterodimer, also functions during meiosis to generate crossovers. Its activity requires Exo1 as well as the MutSγ heterodimer (Msh4–Msh5). Crossovers also require the polo kinase Cdc5 in a way that is poorly understood. We show that Exo1 directly interacts with Cdc5, and that this promotes the activation of MutLγ for crossovers. Since Cdc5 also controls other key meiotic processes, including kinetochores mono-orientation and disassembly of the synaptonemal complex, this direct interaction with the crossover proteins may be a way to coordinate meiotic chromosome segregation events to avoid untimely activation of the MutLγ endonuclease once recruited to future crossover sites.