SSC1 is a gene that encodes a multifunctional mitochondrial heat shock protein that gave rise to SSQ1 by gene duplication in a subset of yeasts. In contrast to the multiple chaperone functions carried out by most heat shock proteins, Ssq1p is specialized in Fe/S cluster assembly. Ssc1p and Ssq1p both participate in the formation of Fe/S clusters and require interaction with Jac1p. Biochemical experiments and genetic manipulation of Saccharomyces cerevisiae have provided evidence that Ssq1p and Jac1p may have coevolved to optimize a specialized interaction. Together, these factors present a unique opportunity to understand how natural selection shapes the functional coevolution of gene duplicates. We hypothesized that the divergence of SSC1 and SSQ1 resulted in the coevolution of the JAC1-SSQ1 pair. Here, we report that, in the presence of a rapidly evolving SSQ1, the average rate of JAC1 evolution has decreased. Our study also supports a burst of adaptive evolution in SSQ1 immediately following its inception. Additionally, both SSC1 and SSQ1 exhibit elevated rates of evolution when co-occurring. When taken together, the signatures of ancestral and present-day selection point to a release from antagonistic pleiotropy that facilitated coevolution between JAC1 and SSQ1. This study offers detailed evidence that the duplication of multifunctional genes allows for the coevolution of interacting proteins to optimize a paired function.