Diversification of the ca. 275,000 extant flowering plant species has been driven in large part by coevolution with animal pollinators. A recurring pattern of pollinator shifts from hummingbird to hawkmoth pollination has characterized plant speciation in many western North American plant taxa, but in the genus Mimulus (monkeyflowers) section Erythranthe the evolution of hawkmoth pollination from hummingbird-pollinated ancestors has not occurred. We manipulated two flower color loci and tested the attractiveness of the resulting four color phenotypes (red, yellow, pink, and white) to naïve hawkmoths (Manduca sexta). Hawkmoths strongly prefer derived colors (yellow, pink, white) over the ancestral red when choosing an initial flower to visit, and generally preferred derived colors when total visits and total visit time were considered, with no hawkmoth preferring ancestral red over derived colors. The simple flower color genetics underlying this innate pollinator preference suggests a potential path for speciation into an unfilled hawkmoth-pollinated niche in Mimulus section Erythranthe, and the deliberate design of a hawkmoth-pollinated flower demonstrates a new, predictive method for studying pollination syndrome evolution.