Precise signaling at the neuromuscular junction (NMJ) is essential for proper muscle contraction. In the <i>Caenorhabditis elegans</i> pharynx, acetylcholine (ACh) released from the MC and M4 motor neurons stimulates two different types of contractions in adjacent muscle cells, termed pumping and isthmus peristalsis. MC stimulates rapid pumping through the nicotinic ACh receptor EAT-2, which is tightly localized at the MC NMJ, and <i>
eat-2</i> mutants exhibit a slow pump rate. Surprisingly, we found that <i>
eat-2</i> mutants also hyperstimulated peristaltic contractions, and these are characterized by increased and prolonged Ca<sup>2+</sup> transients in the isthmus muscles. This hyperstimulation depends on crosstalk with the GAR-3 muscarinic acetylcholine receptor as <i>
gar-3</i> mutation specifically suppressed the prolonged contraction and increased Ca<sup>2+</sup> observed in <i>
eat-2</i> mutant peristalses. Similar GAR-3 dependent hyperstimulation was also observed in mutants lacking the <i>
ace-3</i> acetylcholinesterase, and we suggest that NMJ defects in <i>
eat-2</i> and <i>
ace-3</i> mutants result in ACh stimulation of extrasynaptic GAR-3 receptors in isthmus muscles. <i>
gar-3</i> mutation also suppressed slow larval growth and prolonged lifespan phenotypes that result from dietary restriction in <i>
eat-2</i> mutants, indicating that crosstalk with the GAR-3 receptor has a long-term impact on feeding behavior and <i>
eat-2</i> mutant phenotypes.