Sea stars control hundreds of tube feet to navigate their environment with a rudimentary nervous system. Tube feet are capable of responding to stimuli without descending nervous commands and it is therefore unclear to what extent tactic orientation emerges through the collective action of the tube feet or is guided by central control. We therefore performed behavioral experiments to test models of neuromechanical control in a sea star (Protoreaster nodosus). We found that animals moved rapidly along relatively straight trajectories when exposed to light, but slowly crawled along circuitous paths in random directions in the dark. To remove mechanical interactions with the substrate, we measured the kinematics of tube feet in inverted sea stars that exhibited crawling when in contact with the water's surface. The tube feet throughout the body of these animals moved with power strokes in a similar direction when the animals were exposed to light, which is consistent with central control. This contrasts the variety of directions for power strokes exhibited without illumination. These findings support of a model of navigational control where directionless body motion emerges from collective mechanics in the dark, but is guided by the nervous system when exposed to light. In this manner, sea stars navigate through a combination of collective and central control.