A marine, filamentous, endolithic cyanobacterium, strain BC008, was obtained in pure culture and characterized using a polyphasic approach. BC008 could bore into calcium carbonate minerals (calcite, aragonite) and, weakly, into strontium carbonate (strontianite), but not into other carbonates, phosphates, sulfates, silicates, or oxides, including those of calcium. We describe procedures for its continued cultivation in an actively boring state. BC008 was developmentally complex: it displayed lateral, terminal, and intercalary heterocysts; true branching; trichome tapering; and motile hormogonia. It also displayed considerable morphological plasticity between boring and nonboring modes. Boring brought about a halving of trichome diameter, a marked decrease in the ratio of heterocysts to vegetative cells, and a significant preference for lateral versus terminal heterocyst development. The cytoplasm of vegetative cells was filled with 20 nm thick, nanocompartment-like structures of polyhedral appearance and of unknown function. BC008 was capable of complementary chromatic adaptation but did not produce sheath pigments. When boring, it conformed well morphologically to Lagerheim’s (1886) description of Mastigocoleus testarum, one of the most common and pervasive bioerosive agents of marine carbonates. We propose strain BC008 as type strain for the species. Multigene (16S rRNA, nif H, rbcL) phylogenies confirm that Mastigocoleus is a distinct, deeply branching genus of cyanobacteria that shares affinities and critical traits with two major taxonomic groups in the heterocystous clade (Nostocales and Stigonematales). We provide a revision of the genus and species descriptions based on our strain and findings.