During development, neurons must find their appropriate targets to assemble behavioral circuits. While we know that genes and molecular pathways direct neuronal development, the complexity of this process and the vast number of genes involved, make neuronal development an active area of discovery. Here, we used the relatively simple acoustic startle circuit in the larval zebrafish, a vertebrate model organism, to uncover the role of celsr3 in circuit assembly. Celsr3 is an atypical cadherin known for its role in tissue patterning as part of the planar cell polarity (PCP) pathway. We discovered that celsr3 promotes axon guidance of two neuronal populations in the startle circuit, Mauthner cells, central to the circuit, and spiral fiber neurons which provide excitatory input onto the Mauthners. The acoustic startle circuit underlies the escape response which is critical for survival. Thus, we utilized this behavior to understand how celsr3 promotes startle circuit assembly and the consequences of incorrect assembly on the escape response, highlighting the importance of simple circuits to bridge the gap between genes, circuits, and behavior. Not only must neurons find their appropriate partners during neuronal development, but this challenge can resurface throughout the animal’s life. Axonal connections are vulnerable to damage by injury or disease. To restore function after injury, axons must regrow and find their appropriate partners. Axons in the zebrafish CNS have an incredible ability to regenerate spontaneously, an ability retained in a few mammals. Using an assay for CNS Mauthner axon regeneration, I discovered that Mauthner axon regeneration is biphasic, as axons first grow slowly across the injury gap and subsequently switch to faster rates of axonal regrowth. Importantly, Mauthner axons in celsr3 mutants fail to switch to faster rates and regenerate, revealing that the celsr3-dependent switch in regrowth rates is critical for CNS regeneration. To date, knowledge of the role of Celsr3 and PCP pathway components in regeneration is limited, thus, this work sets the stage to understand if and to what extent, genetic mechanisms of neuronal development are reutilized in axonal regeneration.