TOG family proteins, including the budding yeast Stu2, are essential for the formation of a functional mitotic spindle. Across all eukaryotes, the described functions of this family depend on two microtubule binding elements: TOG domain arrays, and a basic linker domain important for binding the microtubule lattice. Consistently, we find here that Stu2's basic linker is required for its ability to regulate microtubules in vitro, including stimulating microtubule growth, shrinkage, and catastrophe. We furthermore define a region contained within Stu2's basic linker domain as its nuclear localization sequence, and identify phospho-regulation that promotes mitosis-specific nuclear import. Surprisingly, directing nuclear localization is the only function contained within Stu2's basic linker that is required for cell viability, indicating that microtubule lattice binding is not required for Stu2's essential function. Considering that lattice binding is required to stimulate microtubule polymerization and depolymerization in vitro, these established activities are unlikely to be the essential functions carried out by Stu2 in the cell's nucleus.