Increased cardiac contractility during the fight-or-flight response is caused by β-adrenergic augmentation of Ca1.2 voltage-gated calcium channels. However, this augmentation persists in transgenic murine hearts expressing mutant Ca1.2 α and β subunits that can no longer be phosphorylated by protein kinase A-an essential downstream mediator of β-adrenergic signalling-suggesting that non-channel factors are also required. Here we identify the mechanism by which β-adrenergic agonists stimulate voltage-gated calcium channels. We express α or β subunits conjugated to ascorbate peroxidase in mouse hearts, and use multiplexed quantitative proteomics to track hundreds of proteins in the proximity of Ca1.2. We observe that the calcium-channel inhibitor Rad, a monomeric G protein, is enriched in the Ca1.2 microenvironment but is depleted during β-adrenergic stimulation. Phosphorylation by protein kinase A of specific serine residues on Rad decreases its affinity for β subunits and relieves constitutive inhibition of Ca1.2, observed as an increase in channel open probability. Expression of Rad or its homologue Rem in HEK293T cells also imparts stimulation of Ca1.3 and Ca2.2 by protein kinase A, revealing an evolutionarily conserved mechanism that confers adrenergic modulation upon voltage-gated calcium channels.