The study of intellectual humility (IH), which is gaining increasing interest among cognitive scientists, has been dominated by a focus on individuals. We propose that IH operates at the collective level as the tendency of a collective’s members to attend to each other’s intellectual limitations and the limitations of their collective cognitive efforts. Given people’s propensity to better recognize others’ limitations than their own, IH may be more readily achievable in collectives than individuals. We describe the socio-cognitive dynamics that can interfere with collective IH and offer the solution of building intellectually humbling environments that create a culture of IH that can outlast the given membership of a collective. We conclude with promising research directions.