The structures of the chromophore binding pockets in the Pfr states of various bathy and prototypical biliverdin-binding phytochromes were analysed by using a combined spectroscopic-theoretical approach. For the Pfr state of the bathy phytochrome from Pseudomonas aeruginosa (PaBphP) the very good agreement between calculated Raman spectra of the tetrapyrrole cofactor, obtained by quantum-mechanical / molecular-mechanical hybrid methods, and the experimental resonance Raman (RR) spectra confirms important conclusions derived from the previous crystallographic analyses, particularly the ZZEssa configuration of the chromophore and its attachment to the thiol side chain of Cys12 via the exocyclic vinyl group of ring A. The match between the RR spectra of the Pfr states of PaBphP and the bathy phytochrome Agp2 from Agrobacterium tumefaciens indicates very similar structures of the chromophore binding pockets. The homogeneous chromophore conformation in bathy phytochromes is in sharp contrast to the Pfr states of prototypical phytochromes as demonstrated by comparative RR spectroscopic analyses. The Pfr states of prototypical phytochromes, thoroughly studied for Agp1 (A. tumefaciens), display conformational equilibria between two sub-states differing with respect to the CD methine bridge torsional angle and the AB methine bridge geometry. These differences may mainly root in the interactions of the cofactor with the highly conserved Asp194 (PaBphP) that occur via its carboxylate function in bathy phytochromes. The weaker interactions via the carbonyl function in prototypical phytochromes may lead to a higher structural flexibility of the chromophore binding pocket that opens the reaction channel for the thermal (ZZE → ZZZ) Pfr-to-Pr back-conversion.