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Intermediate filaments (IFs) are essential components of the cytoskeleton involved in most cellular functions including cell migration. However, the regulation of IF dynamics is still poorly understood. We found that the tumor suppressor Adenomatous Polyposis Coli (APC), a key regulator of microtubule reorganization during cell migration, directly binds IFs and bridges IFs and microtubules. APC binding to IFs positively regulates their dynamics both in vitro and in vivo. In addition, APC-mediated regulation of IFs is essential for cell migration and the loss or truncation of APC correlates with a disorganization of the IF network in cancer cells. These results point to APC as a crucial regulator of intermediate filament organization and bring new insights into APC function during cell migration.