Cyanobacteria thrive in very diverse environments. In Earth history however, delayed oxygenation has raised questions of growth limitation in ancient environmental conditions. As a single genus, the Thermosynechococcus are known to be cosmopolitan and live in chemically diverse habitats. To understand the genetic basis for this, we compared the protein coding component of Thermosynechococcus genomes. Supplementing the known genetic diversity of Thermosynechococcus, we report draft metagenome-assembled genomes of two Thermosynechococcus recovered from ferrous carbonate hot springs in Japan. We find that as a genus, Thermosynechococcus is genomically conserved, having a small pan-genome with few accessory genes per individual strain and only 18 protein clusters appearing in all Thermosynechococcus but not in any other cyanobacteria in our analysis. Furthermore, by comparing orthologous protein groups, including an analysis of genes encoding proteins with an iron related function (uptake, storage or utilization), no clear differences in genetic content, or adaptive mechanisms could be detected between genus members, despite the range of environments they inhabit. Overall, our results highlight a seemingly innate ability for Thermosynechococcus to inhabit diverse habitats without having undergone substantial genomic adaptation to accommodate this. The finding of Thermosynechococcus in both hot and high iron environments without adaptation recognizable from the perspective of protein coding genes has implications for understanding the basis of thermophily within this clade, and also suggests that ferrous iron in ancient oceans may not have inhibited the proliferation of Cyanobacteria on Earth. The conserved core genome may be indicative of an allopatric lifestyle - or reduced genetic complexity of hot spring habitats relative to other environments.