Mitochondrial　dysfunction　is　interconnected　with　cancer.　Nevertheless,　how　defective　mitochondria　promote　cancer　is　poorly　understood.　We　find　that　mitochondrial　dysfunction　promotes　DNA　damage　under　conditions　of　increased　apoptotic　priming.　Underlying　this　process,　we　reveal　a　key　role　for　mitochondrial　dynamics　in　the　regulation　of　DNA　damage　and　genome　instability.　The　ability　of　mitochondrial　dynamics　to　regulate　oncogenic　DNA　damage　centers　upon　the　control　of　minority　mitochondrial　outer　membrane　permeabilization　(MOMP),　a　process　that　enables　non-lethal　caspase　activation　leading　to　DNA　damage.　Mitochondrial　fusion　suppresses　minority　MOMP　and　its　associated　DNA　damage　by　enabling　homogeneous　mitochondrial　expression　of　anti-apoptotic　BCL-2　proteins.　Finally,　we　find　that　mitochondrial　dysfunction　inhibits　pro-apoptotic　BAX　retrotranslocation,　causing　BAX　mitochondrial　localization　and　thereby　promoting　minority　MOMP.　Unexpectedly,　these　data　reveal　oncogenic　effects　of　mitochondrial　dysfunction　that　are　mediated　via　mitochondrial　dynamics　and　caspase-dependent　DNA　damage.