Numerous non-avian dinosaurs possessed pennaceous feathers on their forelimbs (proto-wings) and tail (caudal plumage). Their functions remain unclear. We propose that the pennaceous feathers were used in displays to flush prey through stimulation of sensory-neural escape pathways in prey, and to provide higher speed and maneuverability during pursuits after prey. We evaluated escape behavior of grasshoppers to the hypothetical visual flush-displays by a robotic dinosaur, and neurophysiological responses of grasshoppers’ escape pathway to computer animations of the hypothetical flush-displays by dinosaurs. We confirmed that prey of small dinosaurs might have escaped more often when proto-wings were present, especially distally and with contrasting patterns, and when caudal plumage, especially of large area, was used during the hypothetical flush-displays. The reinforcing loop between flush and pursue functions could have contributed to the evolution of larger and stiffer feathers for faster running, maneuverability, and stronger flush-displays, promoting foraging based on the flush-pursue strategy. The flush-pursue hypothesis can explain the presence and distribution of the pennaceous feathers, plumage color contrasts, as well as a number of other features observed in early pennaraptorans. This scenario highlights that sensory-neural processes underlying prey’s antipredatory reactions may contribute to the origin of major evolutionary innovations in predators.