Endomesoderm specification by a maternal β-catenin signal and body axis patterning by interpreting a gradient of zygotic Wnt/β-catenin signalling was suggested to predate the split between Bilateria and their sister clade Cnidaria. However, in Cnidaria, the roles of β-catenin signalling in these processes have not been demonstrated directly. Here, by tagging the endogenous β-catenin in the cnidarian Nematostella vectensis, we confirm that its oral-aboral axis is indeed patterned by a gradient of β-catenin signalling. Strikingly, we show that, in contrast to bilaterians, Nematostella endomesoderm specification is repressed by β-catenin and takes place in the maternal nuclear β-catenin-negative part of the embryo. This completely changes the accepted paradigm and suggests that β-catenin-dependent endomesoderm specification was a bilaterian innovation linking endomesoderm specification to the subsequent posterior-anterior patterning.