Vaccinieae is a morphologically diverse and species-rich tribe in the Ericaceae. While the majority of its diversity is tropical, Vaccinieae is best known for temperate crops (i.e., blueberries, cranberries, huckleberries) of the genus Vaccinium. Vaccinium itself has been previously suggested as highly polyphyletic, and taxonomic boundaries of the remaining genera have been untenable. To better understand the extent of polyphyly of Vaccinium in the context of closely related genera, and gain insights into the evolutionary history of Vaccinieae as a whole, we assembled a nuclear dataset for over 200 taxa, representing 30 of the 34 genera in the tribe, and 25 of the 30 sections of Vaccinium. We additionally constructed a plastome dataset for a subset of these taxa. We present results from various phylogenetic and time-calibrated biogeographic analyses to address the following questions: 1–What are the phylogenetic patterns within Vaccinieae? 2–How do the recovered clades compare with current sectional and generic boundaries? 3–Where and when did major dispersal and diversification events take place? We additionally discuss the taxonomic implications of a polyphyletic Vaccinium (and other genera). We recovered seven major clades corresponding to previously delimited genera and sections of Vaccinium and approximately 30 more that do not correspond to previously delimited groups. Instead, groups generally align with geographic boundaries. Biogeographic reconstruction suggests that tropical diversity of Vaccinieae appears to be the result of multiple, independent movements into tropical habitats from temperate, mostly North American ancestors. Divergence time and diversification results reveal dispersal events aligning with major geographic changes such as the uplift of the Andes, and some of these events coincide with increased diversification rate. Traditionally significant morphology that was used to circumscribe many genera and sections did not follow natural groupings in Vaccinieae with the exception of the pseudo-ten-locular ovary, for which we were able to place the evolutionary origin from the five/four locular ovary state. Given the extensive polyphyly of Vaccinium detected here, we recognize several options for reclassification and favor a move to elevate all sections of Vaccinium to the rank of genus, rendering Vaccinium monospecific, including solely the type, Vaccinium uliginosum.