Crossing over is essential for the faithful disjunction of homologous chromosomes during the first meiotic division. Regulatory processes that control crossing over remain poorly characterized. Our recent studies indicate that regulated protein destruction is a key aspect of crossover control. Here, we show that the pro-crossover function of the conserved meiosis-specific recombination factor, MutSγ (a complex of Msh4 and Msh5), requires its stabilization via phosphorylation. Our analysis reveals that Msh4 is an intrinsically unstable protein by virtue of a disordered domain in its N-terminus, which targets it for proteasomal destruction. The degron activity of this domain is attenuated by its phosphorylation, which is essential for the crossover activity of MutSγ. Msh4 phosphorylation requires the initiation of recombination and chromosome synapsis. These and other genetic requirements suggest that Msh4 phosphorylation occurs in situ at sites of recombination. Consistent with this idea, we show that Msh4 phosphorylation is mediated by the chromatin-based kinase, DDK (Dbf4-Dependent Kinase, a.k.a. Cdc7-Dbf4). We suggest a model in which the intrinsic instability of a subset of meiotic recombination factors enables crossover control via differential stabilization at crossover versus non-crossover recombination sites.