How do plants evolve under a geographic mosaic of pollinator faunas? The Grant-Stebbins model depicts pollinator-mediated ecological speciation through the local adaptation to a heterogeneous pollinator landscape. Despite convincing, testing its underlying processes requires the historical patterns of range expansion and the directions of pollinator shifts. In the SE Asian genus Aeschynanthus, the geographic range of its 160 species mostly overlaps with its putative pollinators, sunbirds. A conspicuous exception is A. acuminatus, widespread across mainland East Asia but also occurs in Taiwan, beyond the range of sunbirds. Previous research on the island revealed that it is exclusively pollinated by a group of uncommon avian pollinators, generalist passerines. However, it remains unknown what pollinates the species in mainland Asia, where both sunbirds and generalist passerines are available. In this study, we integrate population genetics with pollination studies to investigate the roles of pollinator shifts and range expansion in the origin of A. acuminatus. Genome-wide SNPs acquired by restriction-site associated DNA (RAD) sequencing revealed a mainland origin, preceding the range expansion to Taiwan. Pollinator observations at 14 populations in 4 geographic areas on both mainland and the island uncovered heterogeneous pollinator assemblages across populations. Evidence from genetic and pollination studies indicates a shift to a generalized pollination system at the species level. The generalization might arise under an unstable pollinator climate in mainland Asia for reproductive assurance. The inclusion of generalist passerine pollinators further allowed its colonization outside sunbird distribution. Our research also sheds light on how pollination systems involving generalist passerines evolve.