In modern life- and medical-sciences major efforts are currently concentrated on creating artificial photoenzymes, consisting of light- oxygen-voltage-sensitive (LOV) domains fused to a target enzyme. Such protein constructs possess great potential for controlling the cell metabolism as well as gene function upon light stimulus. This has recently been impressively demonstrated by designing a novel artificial fusion protein, connecting the AsLOV2-Jα-photosensor from Avena sativa with the Rac1-GTPase (AsLOV2-Jα-Rac1), and by using it, to control the motility of cancer cells from the HeLa-line. Although tremendous progress has been achieved on the generation of such protein constructs, a detailed understanding of their signaling pathway after photoexcitation is still in its infancy. Here, we show through computer simulations of the AsLOV2-Jα-Rac1-photoenzyme that the early processes after formation of the Cys450-FMN-adduct involve the breakage of a H-bond between the carbonyl oxygen FMN-C4O and the amino group of Gln513, followed by a rotational reorientation of its sidechain. This initial event is followed by successive events including β-sheet tightening and transmission of torsional stress along the Iβ-sheet, which leads to the disruption of the Jα-helix from the N-terminal end. Finally, this process triggers the detachment of the AsLOV2-Jα-photosensor from the Rac1-GTPase, ultimately enabling the activation of Rac1 via binding of the effector protein PAK1.