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Drought threatens plant growth and related ecosystem services. The emergence of plant drought stress under edaphic drought is well studied, whilst the importance of atmospheric drought only recently gained momentum. Yet, little is known about the interaction and relative contribution of edaphic and atmospheric drought on the emergence of plant drought stress. We conducted a gradient experiment, fully crossing gravimetric water content (GWC: maximum water holding capacity—permanent wilting point) and vapour pressure deficit (VPD: 1−2.25 kPa) using five wheat varieties from three species (Triticum monococcum, T. durum & T. aestivum). We quantified the occurrence of plant drought stress on molecular (abscisic acid), cellular (stomatal conductance), organ (leaf water potential) and stand level (evapotranspiration). Plant drought stress increased with decreasing GWC across all organizational levels. This effect was magnified nonlinearly by VPD after passing a critical threshold of soil water availability. At around 20%GWC (soil matric potential 0.012 MPa), plants lost their ability to regulate leaf water potential via stomata regulation, followed by the emergence of hydraulic dysfunction. The emergence of plant drought stress is characterized by changing relative contributions of soil versus atmosphere and their non‐linear interaction. This highly non‐linear response is likely to abruptly alter plant‐related ecosystem services in a drying world. Summary statement: Plant drought stress emerges from a nonlinear interaction of soil water availability (here estimated based on gravimetric water content, GWC) and atmospheric water demand (vapour pressure deficit, VPD) with the relative contribution of VPD accelerating below a critical threshold of GWC. [ABSTRACT FROM AUTHOR]