The border between the posterior ectoderm and the endoderm is a location where two germ layers meet and establish an enduring relationship that also later serves, in deuterostomes, as the anatomical site of the anus. In the sea urchin, a prototypic deuterostome, the ectoderm-endoderm boundary is established before gastrulation, and ectodermal cells at the boundary are thought to provide patterning inputs to the underlying mesenchyme. Here we show that a short-range Wnt5 signal from the endoderm actively patterns the adjacent boundary ectoderm. This signal activates a unique subcircuit of the ectoderm gene regulatory network, including the transcription factors IrxA, Nk1, Pax2/5/8 and Lim1, which are ultimately restricted to subregions of the border ectoderm (BE). Surprisingly, Nodal and BMP2/4, previously shown to be activators of ectodermal specification and the secondary embryonic axis, instead restrict the expression of these genes to subregions of the BE. A detailed examination showed that endodermal Wnt5 functions as a short-range signal that activates only a narrow band of ectodermal cells, even though all ectoderm is competent to receive the signal. Thus, cells in the BE integrate positive and negative signals from both the primary and secondary embryonic axes to correctly locate and specify the border ectoderm.