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Inflorescences of flowering plants adopt diverse genetically programmed and environmentally tuned architectures. By contrast, continued maintenance of the stem-cell pool within the apical meristem is unresponsive to environmental cues. Through a combination of modeling and experimentation inArabidopsis, we reveal a negative feedback loop that buffers environmental signals. This loop comprises the determinacy-promoting pioneer transcription factor LEAFY (LFY) and the indeterminacy-promoting transcriptional co-repressor TERMINAL FLOWER1 (TFL1). At the transition to the flower-producing reproductive phase, LFY directly and quantitatively up-regulates expression ofTFL1. TFL1 in turn negatively feeds back onLFYto prevent LFY overaccumulation. This blocks inflorescence termination even under strong florally inductive signals. Our work uncovers a mechanism for robust environmental buffering involving differential responses of two cell populations to the same environmental stimulus.