AbstractAcid–base equilibria of aqueous cellular fluids play a vital role in constituting various signaling and feedback mechanisms in biological systems. To mimic the complex pH‐directed signaling mechanism in laboratory settings, a pH‐responsive vesicular assembly is presented that shows dynamic multicolor fluorescence and size alterations under the influence of a chemically driven pH cycle. The vesicular architecture is a versatile platform for establishing Förster resonance energy transfer (FRET) interactions between multiple donors and acceptor fluorophores. Spontaneously fluctuating interfacial charge of the vesicles during the pH cycle alters the donor fluorophore's emission intensity, affecting the efficiency of FRET interactions among the donor–acceptor pairs. This enables multicolor as well as transient pure white light fluorescence of the vesicles during the pH cycle. The vesicles also display significant size changes in response to varying pH conditions. Furthermore, the vesicles demonstrate excellent adaptability in terms of the lifespan of the oscillatory cycles and the tunability of the fluorescence color transitions.