As you move through an environment, the positions of surrounding objects relative to your body constantly change. Updating these locations is a central feature of situational awareness and readiness to act. Here, we used functional magnetic resonance imaging and a virtual environment to test how the human brain uses optic flow to monitor changing object coordinates. Only activation profiles in the precuneus and the dorsal premotor cortex (PMd) were indicative of an updating process operating on a memorized egocentric map of space. A subsequent eye movement study argued against the alternative explanation that activation in PMd could be driven by oculomotor signals. Finally, introducing a verbal response mode revealed a dissociation between the two regions, with the PMd only showing updating-related responses when participants responded by pointing. We conclude that visual spatial updating relies on the construction of updated representations in the precuneus and the context-dependent planning of motor actions in PMd.