The plant immune system consists of multiple layers of responses targeting various phases of pathogen infection. Here, we provide evidence showing that two responses, one controlling stomatal closure and the other mediated by intracellular receptor proteins, can be regulated by the same proteins but in an antagonistic manner. The HEAT SHOCK COGNATE70 (HSC70), while previously known as a negative regulator of stomatal closure, is a positive regulator of immune responses mediated by the immune receptor protein SUPPRESSOR OF NPR1-1, CONSTITUTIVE1 (SNC1) as well as basal defense responses. In contrast to HSC70, a calcium-binding protein, BONZAI1 (BON1), promotes abscisic acid- and pathogen-triggered stomatal closure in addition to and independent of its previously known negative role in SNC1 regulation. BON1 likely regulates stomatal closure through activating SUPPESSOR OF THE G2 ALLELE OF SKP1 VARIANT B and inhibiting HSC70. New functions of BON1 and HSC70 identified in this study thus reveal opposite effects of each of them on immunity. The opposing roles of these regulators at different phases of plant immune responses exemplify the complexity in immunity regulation and suggest that immune receptors may guard positive regulators functioning at stomatal closure control.