Internal carotid-artery stenosis (ICAS) causes complex and not yet well understood physiological impairments, which currently limits treatment decisions. We present multimodal perfusion and oxygenation-related MRI-data from unilateral asymptomatic ICAS-patients and age-matched healthy controls. The major aim was to investigate hemodynamic impairments in ICAS within individually defined watershed areas (iWSA’s) to account for individual vascular configurations. We found statistically significant lateralization of hemodynamic parameters within iWSA’s - strongest in WM of iWSA’s. Therefore, our iWSA-based approach facilitates detection of even subtle hemodynamic changes in ICAS. Furthermore, we detected spatially widespread capillary flow heterogeneity increases which are promising future treatment indicators.