Synaptic vesicles fuse at specialised active zone membranes often associated with electron dense projections. However, the functional and structural assembly of this specialised compartment during synaptic development and plasticity remains to be characterised. Here, we provide direct evidence that Drosophila Bruchpilot (BRP), a large coiled coil domain protein with homologies to mammalian CAST/ERC/ELKS proteins, is essential for the adequate composition of the active zone to ensure efficient vesicle release. In brp mutants we observed defective active zone membranes, a complete loss of presynaptic dense bodies, and depressed evoked but sustained spontaneous vesicle release. Elevated sensitivity for the Ca²⁺-buffer EGTA together with untypical short-term facilitation indicated that this release defect was caused by an increased distance between Ca²⁺channels and vesicle docking sites. Correspondingly, Ca²⁺-channels were not appropriately clustered at brp mutant synapses. Our results show that dense body formation is linked to the faithful coupling of Ca²⁺-influx with vesicle fusion, while the recruitment of additional vesicles during bursts of activity can persist in the absence of dense bodies at these glutamatergic synapses.