Efficient ATP synthesis requires the coordinated functions of proteins and RNAs produced from the nuclear genome and the mitochondrial genome. Yet, the importance of coevolution between the genomes in maintaining these interactions is debated. In this study, we assess the role of coevolution within populations by comparing the nuclear and mitochondrial genotypes of high and low fitness hybrids between genetically divergent populations of a marine copepod. High fitness hybrids demonstrated elevated mitochondrial ATP synthesis rates and large biases for nuclear alleles from the same population as their mitochondrial genome. These results suggest that selection strongly favors coevolved mitochondrial and nuclear genes in natural populations. Disruption of mitonuclear compatibility, as may occur during secondary contact between populations, results in substantial reductions in hybrid fitness.