β-catenin plays essential roles in cell adhesion and Wnt signaling, while deregulation of β-catenin is associated with multiple diseases including cancers. Here, we report the crystal structures of full-length zebrafish β-catenin and a human β-catenin fragment that contains both the armadillo repeat and the C-terminal domains. Our structures reveal that the N-terminal region of the C-terminal domain, a key component of the C-terminal transactivation domain, forms a long α helix that packs on the C-terminal end of the armadillo repeat domain, and thus forms part of the β-catenin superhelical core. The existence of this helix redefines our view of interactions of β-catenin with some of its critical partners, including ICAT and Chibby, which may form extensive interactions with this C-terminal domain α helix. Our crystallographic and NMR studies also suggest that the unstructured N-terminal and C-terminal tails interact with the ordered armadillo repeat domain in a dynamic and variable manner.