Midbrain dopamine (DA) neurons are diverse with distinct subpopulations being essential for key functions of the brain: nigrostriatal DA neurons for voluntary movement and mesolimbic DA neurons for learning from reward prediction errors. In addition to being primarily associated with distinct senso-motor or limbic cortical-striatal circuits, DA subpopulations also directly communicate with each other via local DA release in the midbrain. While the inhibitory synaptic nature of this dopamine-to-dopamine signaling has been well established, the pre- and postsynaptic identity and logic of connectivity among DA subpopulations are still unresolved. To fill this gap, we combined retrograde tracing with projection-specific optogenetic stimulation of DA neurons and patch-clamp recordings in the adult mouse of either sex. We functionally identified a unidirectional, motor-to-limbic design of the DA synapse in the midbrain. This motor-to-limbic negative feedback connection in the midbrain was independently confirmed by monosynaptic rabies tracing of projection-defined DA subpopulations. This DA synapse might complement the limbic-to-motor striato-nigro-striatal feedforward architecture of the basal ganglia. We identified the pre- and postsynaptic partners of the dopamine-to-dopamine synapse in the midbrain, independently by functional in vitro patch clamp recordings and monosynaptic rabies tracing of identified dopamine subpopulations. This DA synapse is surprisingly circuit-specific with presynaptic DA neurons projecting to the dorsal striatum and post-synaptic DA neurons projecting to the lateral shell of the nucleus accumbens. Thus, this DA synapse establishes a unidirectional, direct communication between the nigro-striatal and the meso-limbic dopamine systems.