Visual behavioral assays in Drosophila melanogaster were initially developed to explore the genetic control of behavior, but have a rich history of providing conceptual openings into diverse questions in cell and developmental biology. Here, we briefly summarize the early efforts to employ three of these behaviors: phototaxis, the UV-visible light choice, and the optomotor response. We then discuss how each of these assays has expanded our understanding of neuronal connection specificity and synaptic function. All of these studies have contributed to the development of sophisticated tools for manipulating gene expression, assessing cell fate specification, and visualizing neuronal development. With these tools in hand, the field is now poised to return to the original goal of understanding visual behavior using genetic approaches.