Echolocation allows bats to occupy diverse nocturnal niches. Bats almost always use echolocation, even when other sensory stimuli are available to guide navigation. Here, using arrays of calibrated infrared cameras and ultrasonic microphones, we demonstrate that hoary bats (Lasiurus cinereus) use previously unknown echolocation behaviours that challenge our current understanding of echolocation. We describe a novel call type (‘micro’ calls) that has three orders of magnitude less sound energy than other bat calls used in open habitats. We also document bats flying close to microphones (less than 3 m) without producing detectable echolocation calls. Acoustic modelling indicates that bats are not producing calls that exceed 70–75 dB at 0.1 m, a level that would have little or no known use for a bat flying in the open at speeds exceeding 7 m s−1. This indicates that hoary bats sometimes fly without echolocation. We speculate that bats reduce echolocation output to avoid eavesdropping by conspecifics during the mating season. These findings might partly explain why tens of thousands of hoary bats are killed by wind turbines each year. They also challenge the long-standing assumption that bats—model organisms for sensory specialization—are reliant on sonar for nocturnal navigation.