<p>Grass stomata are unique in having dumbbell-shaped guard cell anatomy, but the evolutionary context that led to this dramatic anatomical change remains elusive. Here we compared stomatal responses to changes in leaf water status and light across the order Poales, including the closest relatives of grasses which do not have dumbbell-shaped guard cells. Unlike other angiosperms, non-grass Poales have minimal mechanical interactions between guard cells and neighboring epidermal cells. This is surprising because mechanical interactions between these cells increase maximum stomatal aperture and stomatal responsiveness in angiosperms compared to other land plants. Dumbbell-shaped guard cells in grasses are associated with an increased subsidiary cell area into which guard cells can move by displacement when opening. The reemergence of pronounced mechanical interactions between guard cells and subsidiary cells in grasses enhances stomatal sensitivity to environmental signals and may be linked to the ecological success of this lineage.</p>