Cytoplasmic dynein at the cell cortex exerts pulling forces on astral microtubules powering spindle movements during asymmetric cell divisions in a variety of organisms. In budding yeast, the only mechanism of dynein-mediated “cortical pulling" known to exist is thought to occur via side-on interactions (pulling along the lattice of microtubules), as exhibited by sliding of astral microtubules along the cortex during spindle movements across the mother-bud neck. Whether dynein mediates end-on capture-shrinkage of microtubules and how dynein is regulated between side-on and end-on interactions with microtubules are not known. Here we show by direct quantitative imaging that dynein uses end-on pulling mechanism for spindle positioning in cells lacking the cortical endoplasmic reticulum (ER) attachment molecules Scs2 and Scs22. We found that scs2∆ scs22∆ cells displayed a dramatic loss of cortical Num1 patches (dynein anchorage sites), exhibiting fewer than four Num1-GFP patches compared to >10 in wild-type cells. Quantitative immunoblot analysis of Num1 protein revealed that its level was unaffected by deletions of scs2 and scs22, indicating that the loss of Num1-GFP patches was not due to a defect in protein stability. Interestingly, despite being at a lower density, the remaining Num1-GFP patches in scs2∆ scs22∆ cells, seen primarily at the bud tip and the distal end of mother cortex, quantitatively rescued the spindle misorientation and binucleate phenotypes of num1∆, indicating functionality in the dynein-mediated spindle orientation pathway. We found that dynein and dynactin components co-localized with the residual Num1 patches in scs2∆ scs22∆ cells. Strikingly, two-color imaging of spindle movements showed that these Num1 patches mediate capture-shrinkage of astral microtubule plus ends, generating pulling forces that rescue misaligned spindles into the mother-bud neck. Disrupting Num1-dynein interaction (using num1LL mutant allele), but not deleting Kar9 and Bud6 (the canonical capture-shrinkage pathway), abolished end-on capture-shrinkage of microtubule plus ends, demonstrating that dynein mediates spindle movements across the mother-bud neck via end-on interactions in these cells. These findings explain the long-standing enigma reported for yeast dynein from in vitro studies and indicate that cortical ER regulates side-on versus end-on mechanisms of dynein-mediated “cortical pulling”.