Terrestrial productivity today is regulated by stomatal movements, but this has only been the case since “stomatophytes” became dominant on the land 390 million years ago. In this review, we examine evidence for the function of early stomata, found on or near the reproductive structures of bryophyte-like fossils, and consider how this function may have changed through time as vascular plants evolved and diversified. We explore the controversial insights that have come from observing natural variation, rather than genetic manipulation, as a primary tool for understanding the function of the stomatal valve system.