Mitochondria are key components of cellular metabolic processing, providing most of the cellular energy required for survival. The small set of genes located within the mitochondria has recently been the subject of much attention by evolutionary biologists, as a groundswell of studies have documented that allelic variance within the mitochondrial DNA (mtDNA) often confers modifications to the phenotype. Mitochondria have been shown to play an active role in the process of ageing, and mitochondrial allelic variance has been linked to this process. Recent studies suggest that some of this allelic variance is even male-specific in its effects. Here, we use the fruitfly Drosophila melanogaster as a model to advance our understanding of the link between the mitochondrial genotype and phenotype, in young and old flies of each sex. We sequenced full mitochondrial genomes of 13 lines, and examined mtDNA-specific transcriptional profiles of 9 (out of 13) key mitochondrial genes expressed alongside an isogenic nuclear background. We found mitochondrial haplotypic effects on patterns of gene expression within the mitochondrial transcriptome. These effects were in part mediated by both the age and sex of the flies. Furthermore, we identified certain mtDNA SNPs associated with large effects on gene expression. Our results indicate that mtDNA-mediated effects on phenotypic expression are highly dynamic, across the sexes and across ontogeny, and putatively regulated via differential expression among the core set of mtDNA protein-coding genes.