Abstract Twisted intramolecular charge transfer (TICT) dyes are promising candidates for bioimaging and sensing due to their environment‐sensitive fluorescence and large Stokes shifts. However, their inherently low fluorescence quantum yields in aqueous media have limited their practical applications. Here, we present a general supramolecular strategy to transform a broad range of TICT dyes into bright fluorophores with large Stokes shifts. By noncovalently dispersing the dyes into the rigid microdomain of a cyclic peptide‐based supramolecular scaffold in water, the formation of the non‐radiative TICT state is effectively suppressed. The resulting supramolecular TICT dyes exhibit dramatically enhanced fluorescence quantum yields (up to 42.3%), while preserving large Stokes shifts of up to 107 nm. Particularly, supramolecular TICT dyes emitting in the NIR region display excellent photostability, enabling applications in long‐term bioimaging and single‐excitation multi‐color imaging in live cells. This work offers a versatile and modular supramolecular approach to generate high‐performance fluorophores from otherwise low‐ or non‐emissive TICT dyes, greatly broadening their potential in biological and optical applications.