SignificanceViruses rely on organelle remodeling for their replication and for the spread of infection. Alterations to mitochondrial functions and cellular metabolism are hallmarks of nearly all viral infections. However, how the widely spread HCMV remodels mitochondrial structure and function has presented a conundrum. It remained unclear how HCMV increases mitochondrial bioenergetics despite triggering mitochondrial fragmentation. Using a multidisciplinary approach, we address this question. We establish that the uncharacterized viral protein, pUL13, targets the mitochondria, interacts with the MICOS complex, and is sufficient for increasing oxidative phosphorylation during infection. Our findings provide evidence that viral pathogens have acquired mechanisms for manipulating cristae architecture and ETC function to achieve increased energy production and can have broad implications in understanding virus-driven pathologies.