Abstract  Hypertension is a clinical syndrome characterized by increased arterial tone. Although the mechanisms are varied, the generally accepted view is that increased CaV1.2 channel function is a common feature of this pathological condition. Here, we investigated the mechanisms underlying vascular dysfunction in a mouse model of genetic hypertension. Contrary to expectation, we found that whole‐cell CaV1.2 currents (ICa) were lower in hypertensive (BPH) than normotensive (BPN) myocytes. However, local CaV1.2 sparklet activity was higher in BPH cells, suggesting that the relatively low ICa in these cells was produced by a few hyperactive CaV1.2 channels. Furthermore, our data suggest that while the lower expression of the pore‐forming α1c subunit of CaV1.2 s underlies the lower ICa in BPH myocytes, the increased sparklet activity was due to a different composition in the auxiliary subunits of the CaV1.2 complexes. ICa in BPN cells were produced by channels composed of α1c/α2δ/β3 subunits, while in BPH myocytes currents were likely generated by the opening of channels formed by α1c/α2δ/β2 subunits. In addition, Ca2+ sparks evoked BK currents of lower magnitude in BPH than in BPN myocytes, because BK channels were less sensitive to Ca2+. Our data are consistent with a model in which a decrease in the global number of CaV1.2 currents coexist with the existence of a subpopulation of channels highly active that dominate the resting Ca2+ influx. The decrease in BK channel activity turns ineffective the hyperpolarizing brake and leads BPH myocytes to a more contracted resting state.