Somatodendritic dopamine D2-autoreceptors (D2-ARs) modulate spontaneous activity of most dopamine (DA) midbrain neurons in a negative feedback loop, thereby dampening dopamine release. Differences in functional D2-AR expression have been associated with traits like novelty seeking and vulnerability to drug addiction. Given the age dependency of addiction, we investigated maturation of D2-AR function in DA neurons and its modification by cocaine. In SN DA neurons of adult C57BL/6 mice, D2-ARs were tonically active in vivo, indicated by increased mean firing rates and enhanced burst firing induced by selective inhibition with eticlopride. To mimic tonic DA signaling in vitro, we recorded neuronal activity from midbrain slices and challenged SN DA neurons of adult mice with dopamine, which led to D2-AR-mediated complete inhibition of pacemaker-firing without desensitization. In contrast, we observed significant desensitization of D2-AR-mediated pacemaker inhibition in immature SN DA neurons from juvenile mice. Furthermore, three days after a single in vivo cocaine injection, dopamine-induced pacemaker-inhibition was significantly more robust compared to saline injected controls, resembling the adult phenotype. This cocaine-induced plasticity of D2-AR function was selective for juvenile SN DA neurons and surprisingly was not observed in VTA DA neurons. Our pharmacological experiments indicate a crucial role of Cav1.3 L-type calcium channels and neuronal calcium sensor 1 (NCS-1) as key molecular players for D2-AR plasticity of SN DA neurons. Thus, a single cocaine challenge appears to selectively hasten the maturation of D2-AR function in SN DA neurons in calcium dependent manner, which might be a protective response to prevent habit formation.