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Abstract Understanding how evolution proceeds from molecules to organisms to interactions requires integrative studies spanning biological levels. Linking phenotypes with associated genes and fitness illuminates how adaptive walks move organisms between fitness peaks. Floral evolution can confer rapid reproductive isolation, often converging in association with pollinator guilds. Within the monkeyflowers (Mimulussect.Erythranthe), yellow flowers within red hummingbird-pollinated species have arisen at least twice, suggesting possible pollinator shifts. We compare two yellow-flowered forms ofM. cardinalisandM. verbenaceusto their red counterparts in floral phenotypes, biochemistry, transcriptomic and genomic variation, and pollinator interactions. We find convergence in ongoing adaptive walks of both yellow morphs, with consistent changes in traits of large effect (floral pigments, associated gene expression), resulting in strong preference for yellow flowers by bumblebees. Shifts in scent emission and floral opening size also favor bee adaptation, suggesting smaller-effect steps from hummingbird to bee pollination. By examining intraspecific, incipient pollinator shifts in two related species, we elucidate adaptive walks at early stages, revealing how convergent large effect mutations (floral color) may drive pollinator attraction, followed by smaller effect changes for mechanical fit and reward access. Thus, ongoing adaptive walks may impact reproductive isolation and incipient speciation via convergent evolution.