Respiratory syncytial virus (RSV), a major cause of respiratory infections in infants and the elderly, leads to more deaths than influenza each year, but the details of the impact of RSV-host cell interactions are poorly understood. Here we interrogate the impact of RSV infection on host cell mitochondria. Using high resolution imaging and image analysis, we delineate a striking RSV-induced microtubule- and dynein-dependent mitochondrial perinuclear clustering, followed by asymmetric distribution of mitochondria towards the microtubule-organizing centre. Impaired mitochondrial respiration, loss of mitochondrial membrane potential and increased mitochondrial production of reactive oxygen species (ROS), as assessed by mitochondrial membrane potential- and redox-sensitive dyes, accompany these morphological changes. Importantly, we establish the key importance of mitochondrial redistribution and ROS production to infection by demonstrating that infectious RSV production is effectively suppressed by agents that can either target microtubule integrity, inhibit the microtubule motor dynein, or that act as a mitochondrial antioxidant. Together, the results demonstrate RSV’s ability to co-opt host cell mitochondria, and reveal the RSV-mitochondrial interface as a potential target for future intervention strategies.