Fluorescent proteins with emission beyond 650 nm offer the potential for deeper tissue penetration and may also provide lengthened imaging times. Low temperature experiments on the red fluorescent protein mPlum show a reduced Stokes shift compared to room temperature. This suggests that the flexibility of the chromophore environment is related to the large Stokes shift observed in mPlum. We used molecular dynamics (MD) simulations to investigate the relationship between the flexibility of the chromophore environment and the Stokes shift in mPlum at various temperatures. We also examined the solvation dynamics in a panel of strategic point mutants of residues E16 and I65 proposed to participate in a hydrogen-bonding interaction thought responsible for its red-shifted emission. Variants of the largest Stokes shifts exhibited a facile switching between a direct and water-mediated hydrogen bond between residue 16 and 65. This dynamic model underscores the role of environmental flexibility in the mechanism of excited state solvation and provides a template for engineering next-generation red fluorescent proteins.