Oculomotor studies provide a novel strategy for evaluating the functional integrity of multiple brain systems and cognitive processes in autism. The current study compared pursuit eye movements of 60 high-functioning individuals with autism and 94 intelligence quotient, age and gender matched healthy individuals using ramp and oscillating target tasks. Individuals with autism had normal pursuit latency, but reduced closed-loop pursuit gain when tracking both oscillating and ramp targets. This closed-loop deficit was similar for leftward and rightward pursuit, but the difference between individuals with autism and their age-matched peers was more apparent after mid-adolescence, suggesting reduced maturational achievement of the pursuit system in autism. Individuals with autism also had lower open-loop pursuit gain (initial 100 ms of pursuit) and less accurate initial catch-up saccades during a foveofugal step-ramp task, but these deficits were only seen when targets moved into the right visual field. Pursuit performance in both open- and closed-loop phases was correlated with manual praxis in individuals with autism. Bilateral disturbances in the ability to use internally generated extraretinal signals for closed-loop pursuit implicate frontostriatal or cerebellar circuitry. The hemifield specific deficit in open-loop pursuit demonstrates a lateralized disturbance in the left extrastriate areas that extract visual motion information, or in the transfer of visual motion information to the sensorimotor areas that transform visual information into appropriate oculomotor commands.