Plants have evolved a signalling pathway in which, when one root senses local nitrogen (N) deficiency, nitrate uptake by other roots is enhanced in a complementary manner. This long-range communication, known as systemic N-demand signalling, is triggered when the root-to-shoot mobile signal, C-TERMINALLY ENCODED PEPTIDE (CEP), which is induced in roots under N starvation, is perceived by CEP RECEPTOR 1 (CEPR1) expressed in the leaf phloem. However, the molecular components required for CEP-dependent CEPR1 activation remain unknown. Here we identified a leucine-rich repeat receptor kinase that interacts with CEPR1 in a CEP-dependent manner, which we named CEP RECEPTOR INTERACTOR (CERI). CERI belongs to the last functionally uncharacterized clade within the Arabidopsis leucine-rich repeat receptor kinase subgroup II. Loss of CERI impairs systemic N-demand signalling but does not affect CEPR1-mediated regulation of root system architecture. CERI functions as a co-receptor that confers signalling specificity on CEPR1 by selectively mediating systemic N-demand signalling.