Two visual sensing modalities in insects, the ocelli and compound eyes, provide signals used for flight stabilization and navigation. In this article, a generalized model of the ocellar visual system is developed for a 3-D visual simulation environment based on behavioral, anatomical, and electrophysiological data from several species. A linear measurement model is estimated from Monte Carlo simulation in a cluttered urban environment relating state changes of the vehicle to the outputs of the ocellar model. A fully analog-printed circuit board sensor based on this model is designed and fabricated. Open-loop characterization of the sensor to visual stimuli induced by self motion is performed. Closed-loop stabilizing feedback of the sensor in combination with optic flow sensors is implemented onboard a quadrotor micro-air vehicle and its impulse response is characterized.