Honeybees use wide-field visual motion information to calculate the distance they have flown from the hive, and this information is communicated to conspecifics during the waggle dance. Seed treatment insecticides, including neonicotinoids and novel insecticides like sulfoxaflor, display detrimental effects on wild and managed bees, even when present at sublethal quantities. These effects include deficits in flight navigation and homing ability, and decreased survival of exposed worker bees. Neonicotinoid insecticides disrupt visual motion detection in the locust, resulting in impaired escape behaviors, but it had not previously been shown whether seed treatment insecticides disrupt wide-field motion detection in the honeybee. Here, we show that sublethal exposure to two commonly used insecticides, imidacloprid (a neonicotinoid) and sulfoxaflor, results in impaired optomotor behavior in the honeybee. This behavioral effect correlates with altered stress and detoxification gene expression in the brain. Exposure to sulfoxaflor led to sparse increases in neuronal apoptosis, localized primarily in the optic lobes, however there was no effect of imidacloprid. We propose that exposure to cholinergic insecticides disrupts the honeybee’s ability to accurately encode wide-field visual motion, resulting in impaired optomotor behaviors. These findings provide a novel explanation for previously described effects of neonicotinoid insecticides on navigation and link these effects to sulfoxaflor for which there is a gap in scientific knowledge.