Phytochrome photoperception is a common mechanism for the detection of red and far-red light in bacteria, cyanobacteria, fungi and plants. However, the responses following phytochrome activation appear to be quite diverse between species. Lower plants, such as mosses, show phytochrome-mediated directional responses, namely phototropism and polarotropism. These cannot be explained by nuclear gene regulation and are thought to be triggered by phytochromes in the cytoplasm or at the plasma membrane. In higher plants, similar directional responses are mediated via phototropin, a blue light receptor, with phytochromes mainly controlling morphogenetic responses through gene regulation. However, cytoplasmic phytochrome responses exist in higher plants too, which appear to be intertwined with directional blue light perception. By summarizing the respective findings, a possible conservation of cytoplasmic phytochrome function in higher and lower plants is addressed here.