We reveal a novel mechanism that explains how preparatory activity can evolve in motor-related cortical areas without prematurely inducing movement. The smooth eye movement region of the frontal eye fields (FEF SEM) is a critical node in the neural circuit controlling smooth pursuit eye movement. Preparatory activity evolves in the monkey FEF SEM during fixation in parallel with an objective measure of visual-motor gain. We propose that the use of FEF SEM output as a gain signal rather than a movement command allows for preparation to progress in pursuit without causing movement. We also show that preparatory modulation of firing rate in FEF SEM predicts movement, providing evidence against the ‘movement-null’ space hypothesis as an explanation of how preparatory activity can progress without movement. Finally, there is a partial reorganization of FEF SEM population activity between preparation and movement that would allow for a directionally non-specific component of preparatory visual-motor gain enhancement in pursuit.