Perturbations in chloroplastic processes such as photosynthesis by environmental stimuli are communicated to the nucleus to invoke acclimation responses; this process is termed retrograde signaling. Chloroplast-nuclear retrograde signaling is a key mechanism for inter-organelle communication. We found that 3-phosphoadenosine 5-phosphate (PAP) retrograde signal functions more broadly in guard cells, interacting with abscisic acid (ABA) signaling in Arabidopsis. A combination of genetics, biochemical and electrophysiology approaches show that chloroplast communication via PAP forms a novel secondary pathway in abscisic acid (ABA)-mediated stomatal closure during drought stress. Transcriptome of isolated Arabidopsis mesophyll and guard cells revealed that PAP differentially regulates key ABA signaling components in the wild type, a PAP accumulator – altered expression of APX2 8 (alx8), drought-sensitive Open Stomata 1 (ost1-2), and ost1-2/alx8 double mutant. Moreover, reactive oxygen species, nitric oxide, ion fluxes, and ion channels were found to be differently regulated in guard cells of the four Arabidopsis lines. In summary, PAP may function at downstream of the core ABA reception complex – regulatory component of ABA receptors (RCARs), ABA Insensitive 1 (ABI1) and OST1, therefore bypass those essential components for stomatal closure. We demonstrate how a chloroplast signal can directly intersect with and fine-tune ABA signaling for drought response in Arabidopsis.