Modulation of synaptic transmission is a major mechanism for neural circuit reconfiguration. Neurotransmitter release, and consequently synaptic strength, are regulated by intracellular Ca²⁺ levels in presynaptic terminals. In identified neurons of the lobster pyloric network, we studied localized, voltage-induced Ca²⁺ accumulation and its modulation in varicosities on distal neuritic arborizations, which have previously been shown to be sites of synaptic contacts. We previously demonstrated that dopamine (DA) weakens synaptic output from the pyloric dilator (PD) neuron and strengthens synaptic output from the lateral pyloric (LP) and pyloric constrictor (PY) neurons. Here we show that DA modifies voltage-activated Ca²⁺ accumulation in many varicosities in ways that are consistent with DA’s effects on synaptic transmission: DA elevates Ca²⁺ accumulation in LP and PY varicosities, and reduces Ca²⁺ accumulation in PD varicosities. However, in all three neuron types, we also found varicosities that were unaffected by DA. In the PY neurons, we found that DA can simultaneously increase and decrease voltage-evoked Ca²⁺ accumulation at different varicosities, even within the same neuron. These results suggest that regulation of Ca²⁺ entry is a common mechanism to regulate synaptic strength in the pyloric network. However, voltage-evoked local Ca²⁺ accumulation can be differentially modulated to control Ca²⁺-dependent processes in functionally separate compartments of a single neuron.