Under adverse conditions such as shade or elevated temperatures, cotyledon expansion is reduced and hypocotyl growth is promoted to optimize plant architecture. The mechanisms underlying the repression of cotyledon cell expansion remain unknown. Here, we report that the nuclear abundance of the BES1 transcription factor decreased in the cotyledons and increased in the hypocotyl in Arabidopsis thaliana under shade or warmth. Brassinosteroid levels did not follow the same trend. PIF4 and COP1 increased their nuclear abundance in both organs under shade or warmth. PIF4 directly bound the BES1 promoter to enhance its activity but indirectly reduced BES1 expression. COP1 physically interacted with the BES1 protein, promoting its proteasome degradation in the cotyledons. COP1 had the opposite effect in the hypocotyl, demonstrating organ-specific regulatory networks. Our work indicates that shade or warmth reduces BES1 activity by transcriptional and post-translational regulation to inhibit cotyledon cell expansion. [Display omitted] • Shade or warmth reduces BES1 abundance to restrict cotyledon expansion • Under shade or warmth, COP1 physically interacts with BES1 • COP1 targets BES1 to degradation in the cotyledons, but not in the hypocotyl • Under shade or warmth, PIF4 reduces BES1 expression To face environmental challenges, plants have to adjust the growth of their organs selectively. Costigliolo-Rojas et al. show that the mechanisms of growth regulation involve the same molecular components differentially connected in the cotyledons and hypocotyl. [ABSTRACT FROM AUTHOR]