The outstanding elastomeric properties of natural resilin, an insect protein, have motivated the engineering of resilin‐like polypeptides (RLPs) as a potential material for cardiovascular tissue engineering. The RLPs, which incorporate biofunctional domains for cell‐matrix interactions, are cross‐linked into RLP–PEG hybrid hydrogels via a Michael‐type addition of cysteine residues on the RLP with vinyl sulfones of an end‐functionalized multi‐arm star PEG. Oscillatory rheology indicated the useful mechanical properties of these materials. Assessments of cell viability via confocal microscopy clearly show the successful encapsulation of human aortic adventitial fibroblasts in the three‐dimensional matrices and the adoption of a spread morphology following 7 days of culture. Engineered polypeptide–PEG hydrogels based upon the elastomeric structural protein, resilin, are cross‐linked via Michael‐type addition reaction between cysteine residues of the protein polymer and the end‐functionalized vinyl sulfones of a multi‐arm PEG macromer. The precursors quickly form elastic hydrogels and successfully support the adhesion and spreading of human aortic adventitial fibroblasts.