Most mitochondrial proteins are synthesized in the cytosol and directed into the organelle; matrix proteins contain presequences that guide them through translocases in contact sites of the outer and inner membrane. In contrast, the import of many intermembrane space proteins depends on cysteine residues and the oxidoreductase Mia40. Here, we show that both import machineries can cooperate in the biogenesis of matrix proteins. Mrp10, a conserved protein of the mitochondrial ribosome, interacts with Mia40 during passage into the matrix. Mrp10 contains an unconventional proline-rich matrix-targeting sequence that renders import intermediates accessible to Mia40. Although oxidation of Mrp10 is not essential for its function in mitochondrial translation, the disulfide bonds prevent proteolytic degradation of Mrp10 and thereby counteract instability of the mitochondrial genome. The unconventional import pathway of Mrp10 is presumably part of a quality-control circle that connects mitochondrial ribosome biogenesis to the functionality of the mitochondrial disulfide relay.