Organismal fitness is partly determined by how well the nutritional intake matches sex-specific metabolic requirements. Metabolism itself is underpinned by complex genomic interactions involving products from both nuclear and mitochondrial genomes. Products from these two genomes must coordinate how nutrients are extracted, utilised and recycled; processes vital for fuelling reproduction.  Given the complicated nature of metabolism, it is not well understood how the functioning of these two genomes is modulated by nutrients. Here we use nutritional geometry techniques on Drosophila lines that only differ in their mtDNA, with the aim to understand if there is nutrient-dependent mitochondrial genetic variance for male reproduction. We first find genetic variance for diet consumption, indicating that flies are consuming different amounts of food to meet new physiological requirements. We then find an interaction between mtDNA and diet for fitness, suggesting that the mtDNA plays a role in modulating diet-dependent fitness. Our results enhance our basic understanding of nutritional health and our chimeric genomes.