The ghrelin receptor (GhrelinR) and its related orphan GPR39 each display constitutive signaling, but only GhrelinRs undergo basal internalization. Here we investigate these differences, by considering the roles of the C tail receptor domains for constitutive internalization and activity. Furthermore the interaction between phosphorylated receptors and -arrestin adaptor proteins has been examined. Replacement of the FLAG-tagged GhrelinR C tail with the equivalent GPR39 domain (GhR-39 chimera) preserved G_q signaling. However in contrast to the GhrelinR, GhR-39 receptors exhibited no basal and substantially decreased agonist-induced internalization in transiently transfected HEK293 cells. Internalized GhrelinR and GhR-39 were predominantly localized to recycling compartments, identified with transferrin and the monomeric G proteins Rab5 and Rab11. Both the inverse agonist [D-Arg¹, D-Phe⁵, D-Trp^7,9, Leu¹¹]- substance P, and a naturally occurring mutant GhrelinR(A204E) with eliminated constitutive activity, inhibited basal GhrelinR internalization. Surprisingly we found that non-internalizing GPR39 was highly phosphorylated, and that basal and agonist-induced phosphorylation of the GhR-39 chimera was elevated compared to GhrelinRs. Moreover basal GhrelinR endocytosis occurred without significant phosphorylation, and it was not prevented by co-transfection of a dominant negative -arrestin1(319–418) fragment, nor by expression in -arrestin1/2 double knockout mouse embryonic fibroblasts. In contrast agonist-stimulated GhrelinRs recruited the clathrin adaptor GFP--arrestin2 to endosomes, co-incident with increased receptor phosphorylation. Thus GhrelinR internalization to recycling compartments depends on C terminal motifs and constitutive activity, but the high levels of GPR39 phosphorylation, and of the GhR-39 chimera, are not sufficient to drive endocytosis. In addition basal GhrelinR internalization occurs independently of -arrestins.