Morphological and molecular studies demonstrate that the tribe Ptiloteae (Ceramiaceae, Ceramiales) is polyphyletic. The Ptiloteae, sensu stricto, occur only in the Northern Hemisphere and all Southern Hemisphere representatives belong in other tribes. Three genera (Euptilota, Seirospora, and Sciurothamnion) are transferred to the Euptiloteae Hommersand et Fredericq, trib. nov., and the Callithamnieae is revised to include three Ptilota‐like genera, Georgiella, Falklandiella, and Diapse, and two new genera. Heteroptilon Hommersand, gen. nov. is erected to receive Euptilota pappeana Kützing 1849 and Aglaothamnion rigidulum De Clerck, Bolton, Anderson et Coppejans 2004 from South Africa, and Aristoptilon Hommersand et W. A. Nelson, gen. nov. is established to receive Euptilota mooreana Lindauer 1949 from New Zealand. The principal difference between the Euptiloteae and the Callithamnieae is seen in the earliest stages after fertilization. The fertilized carpogonium enlarges and forms a pair of tube‐like protuberances directed toward the auxiliary cells that are cut off as connecting cells in the Euptiloteae, whereas in the Callithamnieae the carpogonium usually divides into two cells, each of which cuts off a small connecting cell that fuses with an adjacent enlarging auxiliary cell. Nuclei are terminal in spermatangia of the Euptiloteae, subtended by mucilaginous vesicles, and are medial in the Callithamnieae situated between apical and basal vesicles. The Euptiloteae and Callithamnieae (including the Ptilota‐like members) are each strongly supported in maximum‐likelihood tree topologies resulting from analyses of combined 18S rDNA, 28S rDNA, 16S rDNA, and rbcL data sets. Their sister relationship is also well supported.