Neuronal activity encoding eye position and gaze signals participates in updating the spatial representations found in the posterior parietal cortex and is necessary for spatial accuracy in goal-directed movements. Using retrograde transneuronal transfer of rabies virus in combination with a conventional tracer, we studied direct and polysynaptic inputs to the ventral lateral intraparietal area (LIPv) and medial intraparietal area (MIP) in non-human primates, to identify possible sources of eye position and gaze signals. We found that these areas receive disynaptic inputs from the brainstem horizontal eye position integrator network (nucleus prepositus hypoglossi, PH) via the central lateral and ventral lateral thalamic nuclei. Our findings provide the first demonstration that inputs from the horizontal eye position integrator reach cortical areas. We found important topographical differences between PH populations targeting MIP and LIPv that likely reflect transmission of different types of eye movement signals. LIPv receives projections from the ipsilateral rostral PH, which may transmit ipsilateral eye position signals. In addition to inputs from the rostral PH, MIP receives strong projections from the contralateral caudal PH, which may contribute to both eye position and velocity signals. Unlike the horizontal integrator, we found that the vertical eye position integrator network, the interstitial nucleus of Cajal, does not project to these posterior parietal areas, in keeping with findings that the thalamic nuclei targeting LIPv and MIP receive almost exclusively horizontal oculomotor signals.