Driving a vehicle is an indispensable daily behaviour for many people, yet we know little about how it is supported by the brain. Given that driving in the real world involves the engagement of many cognitive systems that rapidly change to meet varying environmental demands, identifying its neural basis presents substantial problems. By employing a unique combination of functional magnetic resonance imaging (fMRI), an accurate interactive virtual simulation of a bustling central London (UK) and a retrospective verbal report protocol, we surmounted these difficulties. We identified different events that characterise the driving process on a second by second basis and the brain regions that underlie them. Prepared actions such as starting, turning, reversing and stopping were associated with a common network comprised of premotor, parietal and cerebellar regions. Each prepared action also recruited additional brain areas. We also observed unexpected hazardous events such as swerving and avoiding collisions that were associated with activation of lateral occipital and parietal regions, insula, as well as a more posterior region in the medial premotor cortex than prepared actions. By contrast, planning future actions and monitoring fellow road users were associated with activity in superior parietal, lateral occipital cortices and the cerebellum. The anterior pre-SMA was also recruited during action planning. The right lateral prefrontal cortex was specifically engaged during the processing of road traffic rules. By systematically characterising the brain dynamics underlying naturalistic driving behaviour in a real city, our findings may have implications for how driving competence is considered in the context of neurological damage.