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Abstract PremiseThe ~140 species ofLoniceraare characterized by variously fused leaves, bracteoles, and ovaries, making it a model system for studying the evolution and development of organ fusion. However, previous phylogenetic analyses, based mainly on chloroplast DNA markers, have yielded uncertain and conflicting results. A well‐supported phylogeny ofLonicerawill allow us to trace the evolutionary history of organ fusion. MethodsWe inferred the phylogeny ofLonicerausing restriction site–associated DNA sequencing (RADSeq), sampling all major clades and 18 of the 23 subsections. This provided the basis for inferring the evolution of five fusion‐related traits. ResultsRADSeq data yielded a well‐resolved and well‐supported phylogeny. The two traditionally recognized subgenera (PericlymenumandChamaecerasus), three of the four sections (Isoxylosteum,Coeloxylosteum, andNintooa), and half of the subsections sampled were recovered as monophyletic. However, the large and heterogeneous sectionIsikawas strongly supported as paraphyletic.Nintooa, a clade of ~22 mostly vine‐forming species, includingL. japonica, was recovered in a novel position, raising the possibility of cytonuclear discordance. We document the parallel evolution of fused leaves, bracteoles, and ovaries, with rare reversals. Most strikingly, complete cupules, in which four fused bracteoles completely enclose two unfused ovaries, arose at least three times. Surprisingly, these appear to have evolved directly from ancestors with free bracteoles instead of partial cupules. ConclusionsWe provide the most comprehensive and well‐supported phylogeny ofLonicerato date. Our inference of multiple evolutionary shifts in organ fusion provides a solid foundation for in depth developmental and functional analyses.