Voltage-dependent Ca²⁺ channels contribute to neurotransmitter release, integration of synaptic information, and gene regulation within neurons. Thus, understanding where diverse Ca²⁺ channels are expressed is an important step towards understanding neuronal function within a network. Drosophila provides a useful model for exploring the function of voltage-dependent Ca²⁺ channels in an intact system, but Ca²⁺ currents within the central processes of Drosophila neurons in situ have not been well described. The aim of this study was to characterize voltage-dependent Ca²⁺ currents in situ from identified larval motoneurons. Whole-cell recordings from the somata of identified motoneurons revealed a significant influence of extracellular Ca²⁺ on spike shape and firing rate. Using whole cell voltage clamp, along with blockers of Na⁺ and K⁺ channels, a Ca²⁺ dependent inward current was isolated. The Drosophila genome contains three genes with homology to vertebrate voltage-dependent Ca²⁺ channels: Dmca1A, Dmca1D, and Dm1G. We used mutants of Dmca1A and Dmca1D, as well as targeted expression of an RNAi transgene to Dmca1D to determine the genes responsible for the voltage-dependent Ca²⁺ current recorded from two identified motoneurons. Our results implicate Dmca1D as the major contributor to the voltage-dependent Ca²⁺ current recorded from the somatodendritic processes of motoneurons, whereas Dmca1A has previously been localized to the presynaptic terminal where it is essential for neurotransmitter release. Altered firing properties in cells from both Dmca1D and Dmca1A mutants indicate a role for both genes in shaping firing properties.