The mechanism of stomatal function (control of gas flux through the plant surface via regulation of pore size) is fundamentally mechanical. The material properties of the pore-forming guard cells must play a key role in setting the dynamics and degree of stomatal opening/closure, but our understanding of the molecular players involved and resultant mechanical performance has remained limited. The application of indentation techniques and computational modelling, combined with molecular tools for imaging and manipulating guard cells and their constituent cell walls, has opened the way to a systems approach to analysing this problem. The outcomes of these investigations have led to a reassessment of accepted paradigms and are providing a new understanding of the mechanism of stomatal mechanics. Combined measurement and manipulation of guard cell mechanics, via manipulation of the cell wall, along with computational modelling of the cellular complex, is challenging textbook descriptions of how stomata work. Finite element modelling supports an important role for cellulose-based anisotropy in the wall in guard cell movement. Imaging the guard cell wall reveals novel patterns of molecular components and changing these patterns alters stomatal function. Atomic force microscopy reveals polar stiffening of stomata, which modelling and experimentation reveal facilitates stomatal opening. Radial stiffening of the guard cells is not required for stomatal opening.