We present the first comprehensive multiscale computational investigation of Resonance Raman, absorption and Circular Dichroism spectra of the resting state of the Deinococcus radiodurans phytochrome. The spectra are simulated in all their components, namely the energy position and the lineshapes of both the far-red and the blue bands. To achieve such a goal, we have combined a 4.5 μs MD simulation of the solvated dimeric phytochrome with a hybrid quantum mechanics/molecular mechanics (QM/MM) model, which accounts for both electrostatic and mutual polarization effects between the QM and the MM subsystems. A good agreement with experiments is found for all the three spectra. Moreover, we find a transient H-bond network within the binding pocket of the biliverdin chromophore that, unexpectedly, does not significantly affect the spectra. In parallel, we characterize the vibrations that are more strongly coupled to the biliverdin excitation, confirming the important role of the hydrogen-out-of-plane mode of its vinyl C-H together with the expected C[double bond, length as m-dash]C stretching of the double bond involved in the photoisomerization.