Ca2+ drives aldosterone synthesis in the cytosolic and mitochondrial compartments of the adrenal zona glomerulosa (ZG) cell. Membrane potential across each of these compartments regulates the amplitude of the Ca2+ signal; yet, only plasma membrane ion channels and their role in regulating cell membrane potential have garnered investigative attention as pathological causes of human hyperaldosteronism. Previously, we reported that genetic deletion of TASK-3 channels from mice produces aldosterone excess in the absence of a change in the cell membrane potential of ZG cells. Here, we report using yeast two-hybrid, immunoprecipitation and electron microscopic analyses that TASK-3 channels are resident in mitochondria, where they regulate mitochondrial morphology, mitochondrial membrane potential (mitoVm) and aldosterone production. This study provides proof-of-principle that mitochondrial K+ channels, by modulating inner mitochondrial membrane morphology and mitoVm, have the ability to play a pathological role in aldosterone dysregulation in steroidogenic cells.