Diversification of the ca. 250,000 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, white) to naïve hawkmoths. Hawkmoths strongly prefer derived colors (yellow, pink, white) over the ancestral red, and prefer the two-locus change (white) to either of the single-locus changes (yellow, pink). The simple flower color genetics underlying this innate pollinator preference suggests a potential path for speciation into an unfilled hawkmoth-pollinated niche, and the deliberate design of a hawkmoth-pollinated flower demonstrates a new, predictive method for studying pollination syndrome evolution.