<p>Phytochrome A (phyA) and phyB are red and far-red photoreceptors that interact with PHYTOCHROME-INTERACTING FACTORs (PIFs) via active phyA-binding (APA) or active phyB-binding (APB) motifs. While APB interacts with the N-terminal photosensory module of phyB (phyB^PSM), it remains unclear whether APA interacts with phyA^PSM. We report that both phyA and phyB interact with APA through C-terminal output module of phy (phy^OPM), while phyB interacts additionally with APB through phyB^PSM. Marchantia Mp-phy also interacts with PIFs via the phy^OPM-APA interaction. The phyB^OPM-APA interaction promotes PIF3 degradation but not mutual phyB destruction. The full-length phy-APA interaction is light-dependent, whereas the underlying phy^OPM-APA interaction is not. We show that the Pr form, not the Pfr, of phy^PSM competes with APA for phy^OPM binding, explaining how the light-dependent phy-APA interaction arises from the light-independent phy^OPM-APA interaction. Together, our results suggest that the phy^OPM-APA interaction is an ancient feature conserved in both Arabidopsis phyA, phyB and Marchantia Mp-phy.</p>