The heterotrimeric guanine nucleotide-binding protein (G-protein) has been demonstrated to mediate various signaling pathways in plants. However, its role in phytochrome A (phyA) signaling remains elusive. In this study, we discover a new phyA-mediated phenotype designated far-red irradiation (FR) preconditioned cell death, which occurs only in the hypocotyls of FR-grown seedlings following exposure to white light (WL). The cell death is mitigated in the Ga mutant gpa1 but aggravated in the Gbeta mutant agb1 in comparison with the wild type (WT), indicative of antagonistic roles of GPA1 and AGB1 in the phyA-mediated cell-death pathway. Further investigation indicates that FR-induced accumulation of nonphotoconvertible protochlorophyllide (Pchlide633), which generates reactive oxygen species (ROS) on exposure to WL, is required for FR-preconditioned cell death. Moreover, ROS is mainly detected in chloroplasts using the fluorescent probe. Interestingly, the application of H2O2 to dark-grown seedlings results in a phenotype similar to FR-preconditioned cell death. This reveals that ROS is a critical mediator for the cell death. In addition, we observe that agb1 is more sensitive to H2O2 than WT seedlings, indicating that the G-protein may also modify the sensitivity of the seedlings to ROS stress. Taking these results together, we infer that the G-protein may be involved in the phyA signaling pathway to regulate FR-preconditioned cell death of Arabidopsis hypocotyls. A possible mechanism underlying the involvement of the G-protein in phyA signaling is discussed in this study.