Multiple neurodegenerative diseases, collectively referred to as tauopathies, are characterized by the deposition of insoluble tau aggregates in the brain. These histopathological observations have inspired studies aimed at understanding the mechanisms that normally regulate tau solubility and turnover. From these efforts, it has become clear that a subset of molecular chaperones, including members of the heat shock protein 70 (Hsp70) and heat shock protein 90 (Hsp90) classes, play especially important roles in tau quality control. These chaperones seem to recognize tau upon its release from microtubules, after which they enact quality control decisions that either promote tau rebinding or facilitate its degradation. Here, we review these findings and present a unified view of how Hsp70, Hsp90, and their co-chaperones work together to coordinate healthy tau proteostasis. In this framework, we also discuss how chaperones might be used as potential drug targets for restoring normal tau levels in tauopathy patients. Finally, we discuss the challenges inherent in achieving this goal and speculate about potential research avenues to clarify remaining questions about achieving safety and selectivity.