The macaque monkey’s ventral intraparietal area (VIP) in the intraparietal sulcus (IPS) responds to visual, vestibular, tactile, and auditory signals and is involved in higher cognitive functions, including the processing of peripersonal space. In humans, VIP appears to have expanded into three functionally distinct regions. Macaque VIP has been divided cytoarchitonically into medial and lateral parts; however, no functional specialization has so far been associated with this anatomical division. Functional MRI suggests a functional gradient along the anterior-posterior axis of the macaque IPS: anterior VIP shows visio-tactile properties and face preference, whereas posterior VIP responds to large-field visual dynamic stimuli. This functional distinction matches with functional differences among the three human VIP regions, suggesting that a regional specialization may also exist within macaque VIP. Here, we characterized the macaque ipsilateral, whole-brain functional connectivity, assessed during awake resting state, along VIP’s anterior-posterior axis by dividing VIP into three regions of interest (ROIs). The functional connectivity profiles of the three VIP ROIs resembled anatomical connectivity profiles obtained by chemical tracing. Anterior VIP was functionally connected to regions associated with motor, tactile, and proprioceptive processing and with regions involved in reaching, grasping, and processing peripersonal space. Posterior VIP had the strongest functional connectivity to regions involved in motion processing and eye movements. These profiles are consistent with the connectivity profiles of the anterior and posterior VIP areas identified in humans. Intermediate VIP did not exhibit specific connectivity profiles. Viewed together, resting-state functional connectivity, task-related fMRI, and anatomical tracing consistently suggest specific functional specializations of macaque anterior and posterior VIP.