Successful navigation through the world requires accurate estimation of one’s own speed. To derive this estimate, animals integrate visual speed gauged from optic flow and run speed gauged from proprioceptive and locomotor systems. The primary visual cortex (V1) carries signals related to visual speed, and its responses are also affected by run speed. To study how V1 combines these signals during navigation, we recorded from mice that traversed a virtual environment. Nearly half of the V1 neurons were reliably driven by combinations of visual speed and run speed. These neurons performed a weighted sum of the two speeds. The weights were diverse across neurons, and typically positive. As a population, V1 neurons predicted a linear combination of visual and run speed better than visual or run speeds alone. These data indicate that V1 in the mouse participates in a multimodal processing system that integrates visual motion and locomotion during navigation.