Stomatal opening and closure depends on changes in turgor pressure acting within guard cells to alter cell shape 1. The extent of these shape changes is limited by the mechanical properties of the cells, which will be largely dependent on the structure of the cell walls. Although it has long been observed that guard cells are anisotropic due to differential thickening and the orientation of cellulose microfibrils 2, our understanding of the composition of the cell wall that allows them to undergo repeated swelling and deflation remains surprisingly poor. Here, we show that the walls of guard cells are rich in un-esterified pectins. We identify a pectin methylesterase gene, PME6, which is highly expressed in guard cells and required for stomatal function. pme6-1 mutant guard cells have walls enriched in methyl-esterified pectin and show a decreased dynamic range in response to triggers of stomatal opening/closure, including elevated osmoticum, suggesting that abrogation of stomatal function reflects a mechanical change in the guard cell wall. Altered stomatal function leads to increased conductance and evaporative cooling, as well as decreased plant growth. The growth defect of the pme6-1 mutant is rescued by maintaining the plants in elevated CO2, substantiating gas exchange analyses, indicating that the mutant stomata can bestow an improved assimilation rate. Restoration of PME6 rescues guard cell wall pectin methyl-esterification status, stomatal function, and plant growth. Our results establish a link between gene expression in guard cells and their cell wall properties, with a corresponding effect on stomatal function and plant physiology. Display omitted •The guard cell wall is distinguished by a relatively low level of methylated pectin•Increased methyl pectin leads to stomata with a smaller dynamic range of movement•These plants show increased evaporative cooling and decreased growth under drought•Elevated CO2 restores mutant plant growth to normal Guard cell wall mechanics must play a role in setting the dynamics of stomatal movement. Amsbury et al. show that the degree of pectin methylation in the wall sets the range of cell swelling, with consequences for plant water use and growth being dependent on CO2 level. Stomatal mechanics are likely to influence plant response to climate change.