Throughout the animal kingdom, neuropeptide signaling mediates many survival-promoting behaviors including foraging and the escape response. Even in traditional model organisms like Caenorhabditis elegans, however, the expression and function of several neuropeptide G-protein coupled receptors (GPCRs) remain uncharacterized. Here, we combine molecular genetics and high-throughput behavioral screening to reveal a novel conserved behavioral role for the nematode interneuron neuropeptide receptor FRPR-14. We systematically screened 21 CRISPR/Cas9-generated putative GPCR null mutants using two behavioral paradigms, the posterior light touch-induced response and freely-moving locomotion tracking assays. Although a third of mutants had at least one phenotype, only the frpr-14 mutant was defective in both. A frpr-14 GFP reporter was expressed in the AVJ and AIB interneurons, both of which are presynaptic to several command interneurons. However, only AVJ-specific frpr-14 cDNA expression was sufficient to rescue the full repertoire of mutant phenotypes. We next applied a comparative approach by studying the homologous Cbr-frpr-14 in Caenorhabditis briggsae. A Cbr-frpr-14 GFP reporter showed expression in a single pair of interneurons with strikingly similar morphology and relative anatomical position as the C. elegans AVJ neurons. While C. elegans AVJ-specific expression of Cbr-frpr-14 cDNA rescued all mutant phenotypes, a putative Cbr-frpr-14 null mutant was only defective in the posterior light touch-induced response. We conclude that although FRPR-14’s function at the cellular level is evolutionarily-conserved, this is less evident at the organismal level likely due to differing gene expression patterns and neural architecture between species.