CONSTITUTIVE PHOTOMORPHOGENIC 1 (COP1) represses photomorphogenesis in darkness by targeting nuclear-localized transcription factors to proteasome-mediated degradation. Upon light exposure, COP1 migrates to the cytosol allowing photomorphogenesis to proceed but the residual nuclear pool down-regulates light signaling mediated by phytochrome A. Here we show that weak alleles of cop1 exhibit reverse photomorphogenic responses i.e. reduced rather than enhanced cotyledon unfolding under red light compared to darkness. Conversely, COP1 overexpressors which de-etiolate poorly under blue or far-red light, showed enhanced photomorphogenesis under red light. The positive relationship between COP1 and photomorphogenic response required phytochrome B. Thus, genetic manipulation of COP1 levels differentially affects phytochrome A- compared to phytochrome B-mediated responses. We hypothesize that COP1 could be involved in degradation of negative regulators of photomorphogenesis or in transcriptional activation, as observed for some E3 ligases in mammalian development.