For animals and machines alike, maintaining balance during flight is a crucial and demanding task. The need for airplane flight stability led to a schism between aviators who sought built-in, or passive, stability and those who emphasized the need for active controls. How has this tension played out for the first flyers, the insects? Our group combines table-top experiments on fruit flies and lap-top physically-based simulations to study insect flight stability and control. First, we show how directly perturbing the flight of insects unlocks the physics of flapping-wing flight and also reveals some remarkable properties of these critters’ sensory-neural systems. Second, we argue that these sophisticated fight control systems are largely sculpted by the physical requirement of stability. This idea leads to a general theory that links the body plans of insects with the controllers that must suppress the growth of instabilities, and we apply this theory to a variety of modern insects, flapping-wing robots, and even the prehistoric insects that were the first to take to the air.