The integration of conflicting signals in response to environmental constraints is essential to efficient plant growth and development. The light-dependent and the stress hormone abscisic acid (ABA)-dependent signaling pathways play opposite roles in many aspects of plant development. While these pathways have been extensively studied, the complex nature of their molecular dialogue is still obscure. When mobilized by the Arabidopsis thaliana β-glucosidase 1 (AtBG1), the glucose ester-conjugated inactive form of ABA has proven to be a source of the active hormone that is essential for the adaptation of the plant to water deficit, as evidenced by the impaired stomatal closure of atbg1 mutants in response to water stress. In a suppressor screen designed to identify the molecular components of AtBG1-associated physiological and developmental mechanisms, we identified the mutation variant of AtBG1 traits (vat1), a new mutant allele of the red light/far-red light photoreceptor PHYTOCHROME B (PHYB). Our study reveals that atbg1 plants harbor increased stomatal density in addition to impaired stomatal closure. We also provide evidence that the vat1/phyb mutation can restore the apparent transpiration of the atbg1 mutant by decreasing stomatal aperture and restoring a stomatal density similar to wild-type plants. Expression of key regulators of stomatal development showed a crosstalk between AtBG1-mediated ABA signaling and PHYB-mediated stomatal development. We conclude that the AtBG1-dependent regulation of ABA homeostasis and the PHYB-mediated light signaling pathways act antagonistically in the control of stomatal development.