AbstractThe use of a template that bears pre‐programmed receptor sites for selectively accommodating chromophores at given positions is an attractive approach for engineering artificial‐light‐harvesting systems. Indulging this line of thought, this work tackles the creation of tailored antenna architectures with yellow, red and blue chromophores, exploiting three dynamic covalent reactions simultaneously, namely disulfide exchange, acyl hydrazone, and boronic ester formations. The effect of various structural modifications, such as the chromophores as well as their spatial organization (distance, orientation, order) on the energy transfer within the antennas was studied by means of steady‐state UV/Vis absorption and fluorescence spectroscopies. This systematic study allowed for a significant improvement of the energy‐transfer efficiencies to a noticeable 22 and 15 % for the yellow and red donors, respectively, across the chromophores to the blue acceptor. Metadynamics simulations suggested that the conformational properties of the antennas are driven by intramolecular chromophoric stacking interactions that, upon forcing the α‐helix to fold on itself, annul any effects deriving from the programming of the spatial arrangement of the receptor sides in the peptide backbone.