In face-to-face communication, recurring intervals of mutual gaze allow listeners to provide speakers with visual feedback (e.g. nodding). Here, we investigate the potential feedback function of one of the subtlest of human movements—eye blinking. While blinking tends to be subliminal, the significance of mutual gaze in human interaction raises the question whether the interruption of mutual gaze through blinking may also be communicative. To answer this question, we developed a novel, virtual reality-based experimental paradigm, which enabled us to selectively manipulate blinking in a virtual listener, creating small differences in blink duration resulting in ‘short’ (208 ms) and ‘long’ (607 ms) blinks. We found that speakers unconsciously took into account the subtle differences in listeners’ blink duration, producing substantially shorter answers in response to long listener blinks. Our findings suggest that, in addition to physiological, perceptual and cognitive functions, listener blinks are also perceived as communicative signals, directly influencing speakers’ communicative behavior in face-to-face communication. More generally, these findings may be interpreted as shedding new light on the evolutionary origins of mental-state signaling, which is a crucial ingredient for achieving mutual understanding in everyday social interaction.