Dissolved copper is an increasingly common non–point source contaminant in urban and urbanizing watersheds. In the present study, we investigated the sublethal effects of dissolved copper on the peripheral mechanosensory system, or lateral line, of larval zebrafish (Danio rerio). Zebrafish larvae were exposed to copper (0–65 μg/L), and the cytotoxic responses of individual lateral line receptor neurons were examined using a combination of in vivo fluorescence imaging, confocal microscopy, scanning electron microscopy, and conventional histology. Dissolved copper triggered a dose‐dependent loss of neurons in identified lateral line neuromasts at concentrations ≥20 μg/L. The onset of cell death in the larval mechanosensory system was rapid (<1 h). When copper‐exposed zebrafish were transferred to clean water, the lateral line regenerated over the course of 2 d. In contrast, the lateral line of larvae exposed continuously to dissolved copper (50 μg/L) for 3 d did not recover. Collectively, these results show that peripheral mechanosensory neurons are vulnerable to the neurotoxic effects of copper. Consequently, dissolved copper in non‐point source storm‐water runoff has the potential to interfere with rheotaxis, schooling, predator avoidance, and other mechanosensory‐mediated behaviors that are important for the migration and survival of fish.