The segregation of homologous chromosomes in meiosis depends on their ability to locate one another in the nucleus and establish a physical association through crossing over. A tightly regulated number of crossovers (COs) emerges following repair of induced DNA double‐strand breaks by homologous recombination (HR), but the process of how HR intermediates transition into COs is still poorly understood. Two recent studies by Ahuja et al. and Rao et al. have revealed a role for chromosomally localized proteasomes in choreographing both homologous chromosome pairing and the evolution of HR intermediates into segregation‐competent COs. Using chemical inhibition of the proteasome and mutant analysis, the collective data reveal conserved functions for both the proteasome and a family of E3 ligases that can direct or compete with its activity in ensuring CO formation. Here, we review these findings and the impact of the discovery that protein modification dynamics and proteasomal activity cooperate to regulate key meiotic processes.