Maintaining the integrity of the multiple mitochondrial genomes (mtDNAs) within our cells is critical for the correct function of processes necessary for organismal survival. However, mtDNAs experience molecular damage that accumulates during ageing, which is heritable and can underlie a wide range of diseases. Recently, we have found that the abundance of mtDNA mutations evolves distinctly in different cell types, governed by Pink1/parkin-mediated mitophagy and proteotoxic stress. Now we have uncovered a molecular mechanism that promotes mtDNA repair in response to damage to prolong cell function. In Caenorhabditis elegans, we find that the bZIP transcription factor ATFS-1/Atf5 regulates the balance between transcription and repair of the mtDNA to favour repair by localizing to mitochondria and interfering with the assembly of the mitochondrial pre-initiation transcription complex between HMG-5/TFAM and RPOM-1/mtRNAP. ATFS-1-mediated transcriptional inhibition decreases age-dependent mtDNA molecular damage through the DNA glycosylase NTH-1/NTH1, as well as the helicase TWNK-1/TWNK, resulting in an enhancement in the functional longevity of cells and protection against declines in animal behaviour caused by targeted and severe mtDNA damage. Together, our findings reveal that ATFS-1 acts as a molecular focal point to balance the conflicting demands of mtDNA expression and maintenance in the mitochondria in response to the physiological state of the cell.