Females are often believed to use male ornaments as observable indicators of non-observable male traits. However, if signal form (e.g. coloration) is highly flexible, its link to signal content (e.g. quality) should be unreliable. Therefore, it is often implicitly assumed that signals are heavily constrained and relatively stable over generations. One popular illustration of costly ornaments is carotenoid-based colour signals. Recent but indirect evidence suggest that such signals may in fact evolve rapidly, but this has not been tested experimentally. We exposed large replicated populations of guppies (Poecilia reticulata; effective population sizes >1000) to three environmental conditions in a multi-generation experiment. The treatments differed in the spectral composition of ambient light by using colour filters which affected how male colours were percieved. This, in turn, was expected to lead to male coloration divergence between treatments due to female choice. In addition, the filters affected the micro-flora and -fauna, which are dietary sources of ornamental pigments. Male skin carotenoids were analysed after 3 and 5 generations. In this short time, populations had diverged in male coloration and in the carotenoid composition of sexual ornaments. A second experiment disentangled environmental and genetic effects. Our study demonstrates evolutionary innovation in signal traits, and how dietary-driven responses to environmental change can impact sexual ornaments.