In invertebrates, the direct communication of neighbouring cells is mediated by gap junctions, which are composed of oligomers of the innexin family of transmembrane proteins. Studies of the few known innexin mutants in Drosophila and C. elegans have shown that innexin proteins, which are structurally analogous to the connexins in vertebrates, play a major structural role as gap junctional core components in electric signal transmission. We show that Drosophila innexin 2 mutants display a feeding defect that originates from a failure of epithelial cells to migrate and invaginate during proventriculus organogenesis. The proventriculus is a valve-like organ that regulates food passage from the foregut into the midgut. Immunohistological studies indicate that innexin 2 is functionally required to establish a primordial structure of the proventriculus, the keyhole, during the regionalisation of the embryonic foregut tube, which is under the control of Wingless and Hedgehog signalling. Our genetic lack- and gain-of-function studies, and experiments in Dorsophila tissue culture cells provide strong evidence that innexin 2 is a target gene of Wingless signalling in the proventricular cells. This is the first evidence, to our knowledge, that an invertebrate gap junction gene controls epithelial tissue and organ morphogenesis in response to the conserved WNT signalling cascade.