Meiotic crossover recombination is essential for both accurate chromosome segregation and the generation of new haplotypes for natural selection to act upon. While the conserved role of the ATPase, PCH-2, during meiotic prophase has been enigmatic, a universal phenotype that is observed when pch-2 or its orthologs are mutated is a change in the number and distribution of meiotic crossovers. Here, we show that PCH-2 controls the number and distribution of crossovers by antagonizing crossover formation. This antagonism produces different effects at different stages of meiotic prophase: early in meiotic prophase, PCH-2 prevents double strand breaks from becoming crossovers, limiting crossovers at sites of initial DSB formation and homolog interactions. Later in meiotic prophase, PCH-2 winnows the number of crossover-eligible intermediates, contributing to the reinforcement of crossover-eligible intermediates, designation of crossovers and ultimately, crossover assurance. We also demonstrate that PCH-2 accomplishes this regulation through the meiotic HORMAD, HIM-3. Our data strongly support a model in which PCH-2's conserved role is to remodel meiotic HORMADs throughout meiotic prophase to destabilize crossover-eligible precursors, coordinate meiotic recombination with synapsis, and contribute to the progressive implementation of meiotic recombination, guaranteeing crossover control.