Cyanobacteria comprise an extraordinarily diverse group of microorganisms and, as revealed by increasing molecular information, this biodiversity is even more extensive than previously estimated. In this sense, the cyanobacterial genus Lyngbya is a highly polyphyletic group composed of many unrelated taxa with morphological similarities. In this study, the new genus Dapis was erected from the genus Lyngbya, based on a combined molecular, chemical, and morphological approach. Herein, two new species of cyanobacteria are described: D. pleousa and D. pnigousa. Our analyses found these species to be widely distributed and abundant in tropical and subtropical marine habitats. Seasonally, both species have the ability to form extensive algal blooms in marine habitats: D. pleousa in shallow-water, soft bottom habitats and D. pnigousa on coral reefs below depths of 10 m. Electron microscopy showed that D. pleousa contains gas vesicles, a character not previously reported in Lyngbya. These gas vesicles, in conjunction with a mesh-like network of filaments that trap oxygen released from photosynthesis, provide this species with an unusual mechanism to disperse in coastal marine waters, allowing D. pleousa to be present in both benthic and planktonic forms. In addition, both D. pleousa and D. pnigousa contained nitrogen-fixing genes as well as bioactive secondary metabolites. Several specimens of D. pnigousa biosynthesized the secondary metabolite lyngbic acid, a molecule that has also been isolated from many other marine cyanobacteria. Dapis pleousa consistently produced the secondary metabolite malyngolide, which may provide a promising chemotaxonomic marker for this species.