<p>Optogenetics which involves the use of light to control cell functions on a genetic level has found utility in studying cell physiology, biomaterials and metabolic engineering. <i>S. cerevisiae</i> is an industrially relevant model organism that is used in many applications, but due to the large number of genes required and issues relating to cross-activation between different colours, optogenetics for different wavelengths of light have not been multiplexed in <i>S. cerevisiae</i>. In this paper, we develop a compact red light responsive optogenetic system for <i>S. cerevisiae</i> that requires only a single gene and no exogenous cofactors. Through engineering modular protein domains, we reduce the cross-activation of our system by blue light. We integrate our red light optogenetic system with EL222 blue light optogenetics to establish dual channel optogenetics in <i>S. cerevisiae</i> and demonstrate its utility for engineering biology through the light-based control of flavonoid luteolin synthesis and flocculation for ease of product extraction. We also demonstrate our system’s potential for the development of living materials by producing dual-coloured optogenetic patterns using <i>S. cerevisiae</i>. This work expands optogenetic applications in <i>S. cerevisiae</i> from single-light to multi-light systems, introducing the potential to multiplex different colours of light for dynamic, orthogonal control of separate cell processes.</p>