AbstractIn photosynthesis, pigment–protein complexes achieve outstanding photoinduced charge separation efficiencies through a set of strategies in which excited states delocalization over multiple pigments (“excitons”) and charge‐transfer states play key roles. These concepts, and their implementation in bioinspired artificial systems, are attracting increasing attention due to the vast potential that could be tapped by realizing efficient photochemical reactions. In particular, de novo designed proteins provide a diverse structural toolbox that can be used to manipulate the geometric and electronic properties of bound chromophore molecules. However, achieving excitonic and charge‐transfer states requires closely spaced chromophores, a non‐trivial aspect since a strong binding with the protein matrix needs to be maintained. Here, we show how a general‐purpose artificial protein can be optimized via molecular dynamics simulations to improve its binding capacity of a chlorophyll derivative, achieving complexes in which chromophores form two closely spaced and strongly interacting dimers. Based on spectroscopy results and computational modeling, we demonstrate each dimer is excitonically coupled, and propose they display signatures of charge‐transfer state mixing. This work could open new avenues for the rational design of chromophore–protein complexes with advanced functionalities.