Large, architecturally complex lichen symbioses arose only a few times in evolution, increasing thallus size by orders of magnitude over species from which they evolved. The innovations that enabled symbiotic assemblages to acquire and maintain large size increases are unknown. Morphometric data were mapped against an eight-locus fungal phylogeny across one of the best-sampled thallus size transition events, the origins of the Placopsis lichen symbiosis, and a phylogenetic comparative framework was used to explore the role of nitrogen-fixing cyanobacteria in size differences. Thallus thickness increased by >150% and fruiting body core volume increased nine-fold on average after acquisition of cyanobacteria. Volume of cyanobacteria-containing structures (cephalodia), once acquired, correlates with thallus thickness in both phylogenetic generalised least squares (PGLS) and phylogenetic generalised linear mixed-effects (pGLMM) analyses. The availability of nitrogen appears to be an important factor in the formation of large thalli. Cyanobacterial symbiosis appears to have enabled the lichens to overcome size constraints in oligotrophic environments such as acidic, rain-washed rock surfaces, and in the case of the Placopsis fungal symbiont to have led to an adaptive radiation of more than 60 recognised species. The present data suggest that pre-cyanobacterial symbiotic lineages were constrained to forming a narrow range of phenotypes, so-called cryptic species, leading systematists until now to recognise only six of the 18 species clusters that were identified in Trapelia.