Biochemical and evolutionary interactions between mitochondrial and nuclear genomes (‘mitonuclear interactions’) are proposed evolutionary drivers of sexual reproduction, sexual selection, adaptation, and speciation. We investigated the role of pre-mating isolation in maintaining functional mitonuclear interactions in wild populations bearing diverged proposed co-adapted mitonuclear genotypes. Two lineages of eastern yellow robin Eopsaltria australis—putatively climate-adapted to ’inland’ and ‘coastal’ climates—differ by ~7% of mitochondrial DNA positions, whereas nuclear genome differences are concentrated into a sex-linked region enriched with genes with mitochondrial functions. This pattern can be explained by female-linked selection accompanied by male-mediated gene flow across the narrow hybrid zone where the two lineages coexist. It remains unknown whether lineage divergence is driven by intrinsic incompatibilities (particularly in females, under Haldane’s rule), extrinsic incompatibilities, both, or other drivers. We tested whether lineage divergence could be facilitated by non-random mate-pairing with respect to partners’ mitolineage or nuclear Z sex-chromosome DNA sequences, which differ between the lineages. We used field-, Z-linked-, and mitolineage data from two locations where the lineages hybridize, to test whether females mate disproportionately with (1) males of their own mitolineage and/or bearing similar Z-linked variation, as might be expected if hybrids experience intrinsic incompatibilities, or (2) putatively locally-adapted males, as expected under environmental selection. Comparing field observations with simulations provided no evidence of non-random mating, thus the observed patterns consistent with reduced female gene flow likely occur post-mating. Future tests of female-biased mortality at different life stages and habitat selection may clarify any mechanisms of selection.