Plant genomes encode hundreds of secreted peptides; however, relatively few have been characterised. We report here an uncharacterised, stress‐induced family of plant signalling peptides, which we call CTNIPs. Based on the role of the common co‐receptor BRASSINOSTEROID INSENSITIVE 1‐ASSOCIATED KINASE 1 (BAK1) in CTNIP‐induced responses, we identified in Arabidopsis thaliana the orphan receptor kinase HAESA‐LIKE 3 (HSL3) as the CTNIP receptor via a proteomics approach. CTNIP binding, ligand‐triggered complex formation with BAK1, and induced downstream responses all involve HSL3. Notably, the HSL3‐CTNIP signalling module is evolutionarily conserved amongst most extant angiosperms. The identification of this novel signalling module will further shed light on the diverse functions played by plant signalling peptides and will provide insights into receptor-ligand co‐evolution.