Heterotrimeric G proteins signal at a variety of endomembrane locations, in addition to their canonical function at the cytoplasmic surface of the plasma membrane (PM), where they are activated by cell surface G protein-coupled receptors. Here we focus on signaling at the Golgi, where activates a signaling cascade, ultimately resulting in vesicle fission from the trans-Golgi network (TGN). To develop a novel molecular tool for inhibiting endogenous in a spatial-temporal manner, we take advantage of a lipid association mutant of the widely used inhibitor GRK2ct (GRK2ct-KERE) and the FRB/FKBP heterodimerization system. We show that GRK2ct-KERE cannot inhibit function when expressed in cells, but recruitment to a specific membrane location recovers the ability of GRK2ct-KERE to inhibit signaling. PM-recruited GRK2ct-KERE inhibits lysophosphatidic acid-induced phosphorylation of Akt, whereas Golgi-recruited GRK2ct-KERE inhibits cargo transport from the TGN to the PM. Moreover, we show that Golgi-recruited GRK2ct-KERE inhibits model basolaterally targeted but not apically targeted cargo delivery, for both PM-destined and secretory cargo, providing the first evidence of selectivity in terms of cargo transport regulated by . Last, we show that Golgi fragmentation induced by ilimaquinone and nocodazole is blocked by inhibition, demonstrating that is a key regulator of multiple pathways that impact Golgi morphology. Thus, we have developed a new molecular tool, recruitable GRK2ct-KERE, to modulate signaling at specific subcellular locations, and we demonstrate novel cargo selectivity for regulation of TGN to PM transport and a novel role for in mediating Golgi fragmentation.