The alpha-factor receptor is rapidly hyperphosphorylated on Thr and Ser residues in its hydrophilic C-terminal domain after cells are exposed to pheromone. Mutant receptors in which this domain is altered or removed are biologically active and bind alpha-factor with nearly normal affinity. However, cells expressing the mutant receptors are hypersensitive to pheromone action and appear to be defective in recovery from alpha-factor-induced growth arrest. Mutant receptors with partial C-terminal truncations undergo ligand-induced endocytosis, suggesting that down-regulation of receptor number is not the sole process for adaptation at the receptor level. A mutant receptor lacking the entire C-terminal domain (134 residues) does not display ligand-induced endocytosis. Genetic experiments indicate that the contribution of SST2 function to adaptation does not require the C-terminal domain of the receptor.