Animals that rely on nectar are expected to display floral trait preferences correlating to the signals of nectar source flowers. Batesian mimicry evolves to exploit these pre-existing signal-receiver relationships, attracting pollinators through an adaptive resemblance to specific co-occurring rewarding species. The nectar-feeding long-proboscid flies of South Africa are pollinators for several deceptive orchid species that are putatively Batesian mimics. We tested whether flies’ measured color preference varied among communities providing different nectar-source diets, which would indicate the necessary signal-receiver conditions for the evolution of advergent Batesian mimicry. We introduced artificial rewardless flowers into flowering communities that supported divergent nectar-diets in resident flies and inferred floral trait preferences of a long-proboscid fly species (Prosoeca ganglbaueri) from visitation behavior to these artificial flowers. The experiment showed that the preference of flies for white versus pink was strongly predicted by the colors of flowers most commonly visited by flies at a site. Furthermore, generalization in preference was positively correlated with the variance in nectar-community hue, i.e. flies showed more generalized preference in more spectrally diverse flower communities. The floral tube length of local nectar sources also influenced how readily the flies probed the artificial flowers during attempted foraging. These results support the hypothesis that nectarless orchids pollinated by P. ganglbaueri experience selection for traits that exploit site-specific mutualistic relationships between fly pollinators and their local floral communities.