Interactions with the microtubule drive the working cycle of all kinesins, yet the the structure of the kinesin-microtubule complex remains poorly characterized. We solved a series of 8A-resolution cryo-EM structures representing the microtubule-bound hydrolysis cycles of two different kinesin family members: plus-end directed conventional kinesin, and minus-end directed NCD. These structures reveal that microtubule binding transforms part of the poorly ordered loop L11, located within the switch II nucleotide response element of these kinesins, into a stable extension of the so-called “switch II helix.” We show how this extension likely enables the helix to function as a rigid “relay” element, driving the “power stroke” of both conventional kinesin and NCD. Moreover, binding of ATP analogs in either kinesin variant was associated with a 3% lengthwise contraction of the microtubule lattice. This latter effect may link conventional kinesin and NCD to the microtubule-depolymerizing kinesins.