The rectus extraocular muscle (EOM) pulleys constrain EOM paths. During visual fixation with head immobile, actively-controlled pulleys are known to maintain positions causing EOM pulling directions to change by half the change in eye position. This pulley behavior is consistent with Listings Law (LL) of ocular torsion as observed during fixation, saccades, and pursuit. However, pulley behavior during the vestibulo-ocular reflex (VOR) has been unstudied. This experiment investigated ocular counter-rolling (OCR), a static torsional VOR that violates LL but can be evoked during magnetic resonance imaging (MRI). Tri-planar MRI was performed in 10 adult humans during central target fixation while positioned in right and left side down positions known to evoke static OCR. EOM cross sections and paths were determined from area centroids. Paths were used to locate pulleys in 3-D. Significant (P<0.025) counter-rotational repositioning of the rectus pulley arrays of both orbits was observed in the coronal plane averaging 4.1 deg (maximum 8.7 deg) from right to left side down positions for the inferior, medial, and superior rectus pulleys. There was a trend for the lateral rectus averaging 1.4 deg. Torsional shift of the rectus pulley array was associated with significant contractile cross section changes in the superior and inferior oblique muscles. Torsional rectus pulley shift during OCR, which changes pulling directions of the rectus EOMs, correlates with known insertions of the oblique EOM orbital layers on rectus pulleys. The amount of pulley reconfiguration is roughly half of published values of ocular torsion during static OCR, an arrangement that would cause rectus pulling directions to change by less than half the amount of ocular torsion.