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Abstract Recent studies have uncovered remarkable diversity inDictyonemas.lat. basidiolichens, here recognized as subtribe Dictyonemateae. This group includes five genera and 148 species, but hundreds more await description. The photobionts of these lichens belong toRhizonema, a recently resurrected cyanobacterial genus known by a single species. To further investigate photobiont diversity within Dictyonemateae, we generated 765 new cyanobacterial sequences from 635 specimens collected from 18 countries. The ITS barcoding locus supported the recognition of 200 mycobiont (fungal) species among these samples, but the photobiont diversity was comparatively low. Our analyses revealed three main divisions ofRhizonema, with two repeatedly recovered as monophyletic (proposed as new species), and the third mostly paraphyletic. The paraphyletic lineage corresponds toR. interruptumand partnered with mycobionts from all five genera in Dictyonemateae. There was no evidence of photobiont‐mycobiont co‐speciation, but one of the monophyletic lineages ofRhizonemaappears to partner predominantly with one of the two major clades ofCora(mycobiont) with samples collected largely from the northern Andes. Molecular clock estimations indicate theRhizonemaspecies are much older than the fungal species in the Dictyonemateae, suggesting that these basidiolichens obtained their photobionts from older ascolichen lineages and the photobiont variation in extant lineages of Dictyonemateae is the result of multiple photobiont switches. These results support the hypothesis of lichens representing fungal farmers, in which diverse mycobiont lineages associate with a substantially lower diversity of photobionts by sharing those photobionts best suited for the lichen symbiosis among multiple and often unrelated mycobiont lineages.