Molecular cloning of low‐voltage activated (LVA) T‐type calcium channels has enabled the study of their regulation in heterologous expression systems. Here we investigate the regulation of Ca_v3.2 α₁‐subunits (α1H) by calcium‐ and/or calmodulin‐dependent protein kinase II (CaMKII). 293 cells stably expressing α1H were transiently transfected with CaMKIIγ_C. Using the whole‐cell recording configuration, we observed that elevation of pipette free Ca²⁺ (1 μm) in the presence of CaM (2 μm) increases T‐type channel activity selectively at negative potentials, evoking an 11 mV hyperpolarizing shift in the half‐maximal potential (V_1/2) for activation. The V_1/2 of channel inactivation is not altered by Ca²⁺/CaM. These effects reproduced modulation observed in adrenal zona glomerulosa cells. The potentiation by Ca²⁺/CaM was dependent on the co‐expression of CaMKIIγ_C and required Ca²⁺/CaM‐dependent kinase activity. Peptide (AIP) and lipophilic (KN‐62) protein kinase inhibitors prevented the Ca²⁺/CaM‐induced changes in channel gating without altering basal Ca_v3.2 channel activity (27 nm free Ca²⁺) as did replacing pipette ATP with adenylyl imidodiphosphate (AMP‐PNP), a non‐hydrolysable analogue. CaMKII‐dependent potentiation of channel opening resulted in significant increases in apparent steady‐state open probability (P_o) and sustained channel current at negative voltages. Under identical conditions, CaMKII activation did not regulate the activity of Ca_v3.1 channels, the first cloned member (α1G) of the T‐type Ca²⁺ channel family. Our results provide the first evidence for the differential regulation of two members of the Ca_v3 family by protein kinase activation and the first report reconstituting CaMKII‐dependent regulation of any cloned Ca²⁺ channel.