The vestibulo-ocular reflex (VOR) functions to stabilize gaze when the head moves. The flocculus region (FLR) of the cerebellar cortex, which includes the flocculus and ventral paraflocculus, plays an essential role in modifying signal processing in VOR pathways so that images of interest remain stable on the retina. In squirrel monkeys the firing rate of most FLR Pk cells is modulated during VOR eye movements evoked by passive movement of the head. In this study the responses of 48 FLR Purkinje cells whose firing rate was strongly modulated during VOR evoked by passive whole body rotation or passive head-on-trunk rotation were compared to responses generated during compensatory VOR eye movements evoked by active head movements associated with eye-head saccades. Most (42/48) of the Purkinje cells were insensitive to eye-head saccade-related VOR eye movements. A few (6/48) generated bursts of spikes during saccade-related VOR, but only during on-direction eye movements. Considered as a population FLR Pk cells were less than 5% as responsive to the saccade-related VOR as they were to the VOR evoked by passive head movements. The observations suggest that the FLR has little influence on signal processing in VOR pathways during eye-head saccade-related VOR eye movements. We conclude that the image-stabilizing signals generated by the FLR are highly dependent on the behavioral context, and are called upon primarily when external forces unrelated to self-generated eye and head movements are the cause of image instability.