The adaptive benefit of stomatal crypts remains a matter of controversy. This work studies the effect on gas exchange of cuticular rims that overarch the stomatal pore in the Mediterranean species Quercus coccifera L. growing under Mediterranean (lower relative humidities and high summer temperatures) or oceanic conditions (higher daily relative humidities and mild temperatures). After microscopic assessment of the leaf surfaces and stomatal architecture, the impact of the cuticular ‘cup’ on gas exchange was evaluated by employing three-dimensional finite element models. Here, we provide evidence for a high plasticity of the Q. coccifera cuticular cup, with much larger vents under oceanic conditions compared to small vents under Mediterranean conditions. This structure adds a substantial fixed resistance thereby strongly decreasing gas exchange under Mediterranean conditions. The cuticular cup, which also increases leaf internal humidity, might buffer the rapid changes in vapour pressure deficit (VPD) often observed under Mediterranean conditions. Since water loss of guard and adjacent epidermal cells regulates stomatal aperture, we suggest that this structure allows an efficient regulation of stomatal conductance and optimum use of resources under high VPD. This study provides evidence that plasticity of stomatal architecture can be an important structural component of hydraulic adaptation to different climate conditions.