Protein scaffolds at presynaptic active zone membranes control information transfer at synapses. For scaffold biogenesis and maintenance, scaffold components must be safely transported along axons. A spectrum of kinases was suggested to control transport of scaffold components, but direct kinase/substrate relationships and operational principles steering phosphorylation-dependent active zone protein transport are presently unknown. Here we show that extensive phosphorylation of a 150-residue unstructured region at the N-terminus of the highly elongated BRP/ELKS active zone proteins is crucial for ordered active zone precursor transport. Point mutations that block SRPK79D-kinase-mediated phosphorylation of the BRP/ELKS N-terminus interfered with axonal transport, leading to BRP/ELKS-positive axonal aggregates that also contain additional active zone scaffold proteins. Axonal aggregates formed only in the presence of non-phosphorylatable BRP/ELKS isoforms containing the SRPK79D-targeted N-terminal stretch. We assume that specific active zone proteins are pre-assembled in transport packages and thus co-transported as functional scaffold building blocks. Our results suggest that transient post-translational modification of a discrete unstructured domain of the master scaffold component Bruchpilot blocks oligomerization of such building blocks during their long-range transport.