Dendritic spines are the postsynaptic compartments of glutamatergic synapses in the brain. Their number and shape are subject to change in synaptic plasticity and neurological disorders including autism spectrum disorders and Parkinson’s disease. The L-type calcium channel Ca_V1.3 constitutes an important calcium entry pathway implicated in the regulation of spine morphology. Here we investigated the importance of full-length Ca_V1.3_L and two C-terminally truncated splice variants (Ca_V1.3_42A and Ca_V1.3_43S) and their modulation by densin-180 and shank1b for the morphology of dendritic spines of cultured hippocampal neurons. Live-cell immunofluorescence and super-resolution microscopy of epitope-tagged Ca_V1.3_L revealed its localization at the base-, neck- and head-region of dendritic spines. Expression of the short splice variants or deletion of the C-terminal PDZ-binding motif in Ca_V1.3_L induced aberrant dendritic spine elongation. Similar morphological alterations were induced by co-expression of densin-180 or shank1b with Ca_V1.3_L and correlated with increased Ca_V1.3 currents and dendritic calcium signals in transfected neurons. Together, our findings suggest a key role of Ca_V1.3 in regulating dendritic spine structure. Under physiological conditions it may contribute to the structural plasticity of glutamatergic synapses. Conversely, altered regulation of Ca_V1.3 channels may provide an important mechanism in the development of postsynaptic aberrations associated with neurodegenerative disorders.