Tau was first identified as a protein encoded by the MAPT gene that promotes stabilization and formation of microtubules, cytoskeletal polymers of tubulin essential for survival and intracellular transport of neurons (Weingarten et al., 1975, Franker and Hoogenraad, 2013). Because of tau’s role in neurodegenerative diseases, including Alzheimer’s disease (AD) and other tauopathies (Wang and Mandelkow, 2016), numerous studies have explored the physiological and pathological function, localization, and regulation of tau in the brain. Tau has been canonically regarded as primarily residing in neuronal axons; however, subsequent work has identified tau in a variety of other subcellular domains. Here, we systematically review the reported localization of tau, speculate on the possible functional roles in those areas, and summarize the phosphorylation events implicated in controlling its spatial redistribution. We note that tau is often described as being “mislocalized” to other neuronal compartments, especially in a pathological context. In contrast, we propose the view that tau may perform diverse, physiologically relevant activities in these different subcellular areas, but in a regulated manner that can be uncovered only under the appropriate conditions. Pathology may then emerge from disabling such normal processes or driving them to an excessive level.