A common step in the formation of neural circuits is the conversion of growth cones to presynaptic terminals. Characterizing patterns of global gene expression during this process is problematic due to the cellular diversity of the brain and the complex temporal dynamics of development. Here, we take advantage of the synchronous conversion of Drosophila photoreceptor growth cones into presynaptic terminals to explore global changes in gene expression during presynaptic differentiation. Using a tandemly tagged ribosome trap (T-TRAP) and RNA sequencing (RNA-seq) at multiple developmental times, we observed dramatic changes in coding and non-coding RNAs with presynaptic differentiation. Marked changes in the mRNA encoding transmembrane and secreted proteins occurred preferentially. The 3' UTRs of transcripts encoding synaptic proteins were preferentially lengthened, and these extended UTRs were preferentially enriched for sites recognized by RNA binding proteins. These data provide a rich resource for uncovering the regulatory logic underlying presynaptic differentiation.