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Photoresponsive hydrogels have become invaluable 3D culture matrices for mimicking aspects of the extracellular matrix. Recent efforts have focused on using ultraviolet (UV) light exposure and multifunctional macromers to induce secondary hydrogel crosslinking and dynamic matrix stiffening in the presence of cells. This contribution reports the design of a novel yet simple dynamic poly(ethylene glycol)–peptide hydrogel system through flavin mononucleotide (FMN) induced di‐tyrosine crosslinking. These di‐tyrosine linkages effectively increase hydrogel crosslinking density and elastic modulus. In addition, the degree of stiffening in hydrogels at a fixed PEG macromer content can be readily tuned by controlling FMN concentration or the number of tyrosine residues built‐in to the peptide linker. Furthermore, tyrosine‐bearing pendant biochemical motifs can be spatial‐temporally patterned in the hydrogel network via controlling light exposure through a photomask. The visible light and FMN‐induced tyrosine dimerization process produces a cytocompatible and physiologically relevant degree of stiffening, as shown by changes of cell morphology and gene expression in pancreatic cancer and stromal cells. This new dynamic hydrogel scheme should be highly desirable for researchers seeking a photoresponsive hydrogel system without complicated chemical synthesis and secondary UV light irradiation.