The integration of sensorimotor signals to internally estimate self-movement is critical for spatial perception and motor control. However, which neural circuits accurately track body motion and how these circuits control movement remain unknown. We found that a population of Drosophila neurons that were sensitive to visual flow patterns typically generated during locomotion, the horizontal system (HS) cells, encoded unambiguous quantitative information about the fly's walking behavior independently of vision. Angular and translational velocity signals were integrated with a behavioral-state signal and generated direction-selective and speed-sensitive graded changes in the membrane potential of these non-spiking cells. The nonvisual direction selectivity of HS cells cooperated with their visual selectivity only when the visual input matched that expected from the fly's movements, thereby revealing a circuit for internally monitoring voluntary walking. Furthermore, given that HS cells promoted leg-based turning, the activity of these cells could be used to control forward walking.