We previously reported that parathyroid hormone-related peptide (PTHrP)-induced renal vasodilation is impaired in mature spontaneously hypertensive rats (SHR), through downregulation of the PTH1R, a feature which contributes to the high renal vascular resistance in SHR. Here we asked whether this defect represents a prime determinant in genetic hypertension, or whether it is secondary to angiotensin II (Ang II) and/or to the mechanical forces exerted on the vascular wall. We found that the treatment of SHR with established hypertension by the AT1R antagonist, losartan, reversed the downregulation of PTH1R expression in intrarenal small arteries and restored PTHrP-induced vasodilation in ex vivo perfused kidneys. In contrast, the PTH1R deregulation was not found in intrarenal arteries isolated from prehypertensive SHR. Moreover, this defect which is not seen in extra-renal vessels (aorta, mesenteric arteries) from mature SHR appeared kidney-specific in accordance with the acknowledged enrichment of interstitial Ang II in this organ and its enhancement in SHR. In DOCA-salt rats, an Ang II-independent model of hypertension, renovascular PTH1R expression and related vasodilation were not altered. In SHR-derived renovascular smooth muscle cells (RvSMC), the PTH1R was spontaneously downregulated and its transcript destabilized compared with Wistar RvSMC, both effects being antagonized by losartan. Exogenous Ang II elicited downregulation of PTH1R mRNA in RvSMC from Wistar rats. Together, these data demonstrate that Ang II acts via the AT1R to destabilize PTH1R mRNA in renal vessel in the SHR model of genetic hypertension. This process is kidney-specific and independent from blood pressure increase.