The preglomerular microcirculation of spontaneously hypertensive rats (SHR) is hypersensitive to angiotensin II, and studies show that this is likely due to enhanced convergent signaling between G-protein subunits α_q (Gα_q; released by angiotensin II) and G-protein subunits β (Gβ; released by Gi-coupled receptors) to active phospholipase C (PLC). Here we investigated the molecular basis for the enhanced convergent signaling between Gβ and Gα_q in SHR preglomerular vascular smooth muscle cells (PGVSMCs). Because receptor for activated C kinase 1 (RACK1; scaffolding protein) organizes interactions between Gβ, Gα_q and PLC, we included RACK1 in this investigation. Cell fractionation studies demonstrated increased levels of membrane (but not cytosolic) Gβ, Gα_q, PLCβ₃ and RACK1 in SHR PGVSMCs compared with Wistar-Kyoto rat PGVSMCs. In SHR PGVSMCs, co-immunoprecipitation demonstrated RACK1 binding to Gβ and PLCβ₃, but only at cell membranes. Pertussis toxin (blocks Gβ) and U73122 (blocks PLC) reduced membrane RACK1; however, RACK1 knockdown (shRNA) did not affect membrane levels of Gβ, Gα_q or PLCβ₃. In a novel gel contraction assay RACK1 knockdown in SHR PGVSMCs attenuated contractions to angiotensin II and abrogated the ability of neuropeptide Y (signals via Gβ) to enhance angiotensin II-induced contractions. We conclude that in SHR PGVSMCs the enlarged pool of Gβ and PLCβ₃ recruits RACK1 to membranes and RACK1 then organizes signaling. Consequently, knockdown of RACK1 prevents convergent signaling between angiotensin II and the Gi-pathway. This is the first study to implicate RACK1 in vascular smooth muscle cell contraction and suggests that RACK1 inhibitors could be effective cardiovascular drugs.