Viral rhodopsins are light-gated cation channels representing a novel class ofmicrobial rhodopsins. For viral rhodopsin 1 subfamily members VirChR1 and OLPVR1,channel activity is abolished above a certain calcium concentration. Here we present acalcium-dependent spectroscopic analysis of VirChR1 on the femtosecond to second timescale. Unlike channelrhodopsin-2, VirChR1 possesses two intermediate states P₁ and P₂ onthe ultrafast time scale, similar to J and K in ion-pumping rhodopsins. Subsequently, weobserve multifaceted photocycle kinetics with up to seven intermediate states. Calciumpredominantly affects the last photocycle steps, including the appearance of additional intermediates P₆ᶜᵃ and P₇ representing theblocked channel. Furthermore, the photocycle of the counterion variant D80N is drastically altered, yielding intermediates withdifferent spectra and kinetics compared to those of the wt. These findings demonstrate the central role of the counterion within thedefined reaction sequence of microbial rhodopsins that ultimately defines the protein function.