Self-motion generates visual patterns on the eye that are important for navigation. These optic flow patterns are encoded by the population of local direction–selective cells in the mouse retina, whereas in flies, local direction–selective T4/T5 cells are thought to be uniformly tuned. How complex global motion patterns can be computed downstream is unclear. We show that the population of T4/T5 cells in Drosophila encodes global motion patterns. Whereas the mouse retina encodes four types of optic flow, the fly visual system encodes six. This matches the larger number of degrees of freedom and the increased complexity of translational and rotational motion patterns during flight. The four uniformly tuned T4/T5 subtypes described previously represent a local subset of the population. Thus, a population code for global motion patterns appears to be a general coding principle of visual systems that matches local motion responses to modes of the animal’s movement.