Many animal signals co-occur, and these signals may co-evolve due to their interactive properties. Previous work has demonstrated ecological drivers of evolutionary relationships between signals and the environment, which leads to questions about why specific signal pairs evolved among species that possess multiple signals. We asked whether the coloration of different species was optimized for presentation with its natural behavioral display. We investigated this in “bee” hummingbirds, where males exhibit angle-dependent structurally colored plumage and a stereotyped courtship (shuttle) display, by experimentally creating mis-matches between the behavior and plumage of five species and quantifying how these mis-matches influenced male color appearance during a display. Specifically, we moved the plumage from a given species through the courtship display of other species and quantified the resulting color appearance during the display in order to compare the mis-matched color appearance to each species’ natural color appearance. We found that mis-matches significantly altered display flashiness (% change in coloration during displays) compared to the natural plumage-behavior pairings, and that such departures in flashiness were predicted by differences in shuttle behaviors alone. These results illustrate a tight evolutionary relationship between shuttle displays and color flashiness in these hummingbirds. Further, we found that interspecific variation in male plumage, behavior, and natural color appearance predicted deviations between natural and mis-matched flashy color appearance. Altogether, our work provides a new method for testing coevolution of signals and highlights the complex evolutionary relationships between multiple signals and their interactions.