The ventral intraparietal area (VIP) of the macaque brain is a multimodal cortical region with directionally-selective responses to visual and vestibular stimuli. To explore how these signals contribute to self-motion perception, neural activity in VIP was monitored while macaques performed a fine heading discrimination task based on vestibular, visual, or multisensory cues. For neurons with congruent visual and vestibular heading tuning, discrimination thresholds improved during multisensory stimulation, suggesting that VIP (like area MSTd) may contribute to the improved perceptual discrimination seen during cue combination. Unlike MSTd, however, few VIP neurons showed opposite visual/vestibular tuning over the range of headings relevant to behavior, and those few cells showed reduced sensitivity under cue combination. Our data suggest that the heading tuning of some VIP neurons may be locally remodeled to increase the proportion of cells with congruent tuning over the behaviorally relevant stimulus range. VIP neurons also showed much stronger trial-by-trial correlations with perceptual decisions (choice probabilities, CPs) than MSTd neurons. While this may suggest that VIP neurons are more strongly linked to heading perception, we also find that correlated noise is much stronger among pairs of VIP neurons, with noise correlations averaging 0.14 in VIP as compared to 0.04 in MSTd. Thus, the large CPs in VIP could be a consequence of strong interneuronal correlations. Together, our findings suggest that VIP neurons show specializations that may make them well-equipped to play a role in multisensory integration for heading perception.