Phytochromes are photoreceptors that upon light absorption initiate a physiological reaction cascade. The starting point is the photoisomerization of the tetrapyrrole cofactor in the parent Pr state, followed by thermal relaxation steps culminating in activation of the physiological signal. Here we have employed resonance Raman (RR) spectroscopy to study the chromophore structure in the primary photoproduct Lumi-R, trapped between 130 and 200 K. The investigations covered phytochromes from plants (phyA) and prokaryotes (Cph1, Agp1, CphB, and RpBphP2) including phytochromobilin (PΦB), phycocyanobilin (PCB), and biliverdin (BV). In PΦB- and PCB-binding phyA and Cph1, two Lumi-R states (Lumi-R1, Lumi-R2) were identified and discussed in terms of sequential and parallel reaction models. In Lumi-R1, the chromophore structural changes are restricted to the C-D methine bridge isomerization site but extended throughout the chromophore in Lumi-R2. Formation and decay kinetics as well as photochemical activity depend on the specific protein-chromophore interactions and thus account for the different distribution between Lumi-R1 and Lumi-R2 in the photostationary mixtures of the various PΦB(PCB)-binding phytochromes. For BV-binding bacteriophytochromes, only a single Lumi-R(BV) state was found. In this state, which is similar for Agp1, CphB, and RpBphP2, the chromophore structural changes comprise major torsions of the C-D methine bridge but also perturbations at the A-B methine bridge remote from the isomerization site. The different structures of the photoproducts in PΦB(PCB)-binding phytochromes and BV-binding bacteriophytochromes are attributed to the different disposition of ring D upon isomerization, which leads to distinct protein-chromophore interactions in the Lumi-R states of these two classes of phytochromes.