A RAD-seq phylogeny is presented for the genus Ulmus, and a revised infrageneric classification is given, with keys, descriptions, and range maps for the subgenera and sections. The previously accepted classification was based on a cpDNA phylogeny, but several well-marked clades in the chloroplast phylogeny are not recovered in the RAD-seq phylogeny and do not seem to represent valid clades in the organismal phylogeny. Ordination and STRUCTURE analysis support a broad species concept in Ulmus sect. Foliaceae and demonstrate interspecific hybridization in the section. Several sections of the genus are disjunct between Asia, Europe, and North America, indicating dispersals between the northern continents with inferred dates from ca. 20 Ma to ca. 3 Ma. Morphological variation is discussed, and some characters previously considered characteristic of Ulmus subg. Oreoptelea (narrowly winged achenes, ciliate achene margin) are shared with the unrelated U. villosa. A new subgenus, Ulmus subg. Indoptelea, is described. It can be recognized morphologically by its combination of compact inflorescences with very short pedicels, and samaras with narrow, strongly ciliate wings. It is sister to Ulmus subg. Ulmus, but has a smaller genome than either of the other subgenera.