The smooth pursuit (SP) system can adapt its response to developmental changes, injury and behavioral context. Previous lesion and single unit recording studies show that the macaque cerebellum plays a role in SP initiation, maintenance and adaptation. The aim of this study was to determine the potential role of the DLPN in SP adaptation. The DLPN receives inputs from the cortical SP system and delivers eye and visual motion information to the dorsal/ventral paraflocculus and vermis of the cerebellum. We studied SP adaptation in two juvenile rhesus monkeys (Macaca mulatta), using double-steps of target speed that step-up (10°/s to 30°/s) or step-down (25°/s to 5°/s). We used microinjection of muscimol ( 2%; 0.15µl) to reversibly inactivate (lesion) the DLPN, unilaterally. Following DLPN inactivation, initial ipsilesional SP acceleration (first 100ms) was significantly reduced by 47-74% (P < 0.001; paired t-test) of control values in the single speed step-ramp paradigm. Similarly, ipsilesional steady-state SP velocity was also reduced by 59-78% (P < 0.01; unpaired t-test) of control values. Contralesional SP was not impaired following DLPN inactivation. Control testing showed significant adaptive changes of initial SP eye acceleration after 100 trials in either step-up or step-down paradigms. Following inactivation, during ipsilesional SP, adaptation was impaired in the step-up but not in the step-down paradigm. In contrast, during contralesional tracking, adaptive capability remained in the step-down but not in the step-up paradigm. Therefore, SP adaptation could depend, in part, on direction sensitive eye/visual motion information provided by DLPN neurons to cerebellum.