In the pre-Phylogenomic Analysis era, cyanobacteria of the genus Leptolyngbya have been identified according to such morphological character as thin filaments without true branching; secondary differences concerned ultrastructural and ecological traits. The advent of polyphasic approach allowed to split this genus into monophyletic constituents, and launch many proposals of new ‘Leptolyngbya-like’ taxa. In current interpretation, the genus Leptolyngbya encompasses Leptolyngbya spp. sensu stricto and closely related ‘Leptolyngbya-like’ species of the order Leptolyngbyales. In recent decades, new ‘Leptolyngbya-like’ genera phylogenetically distant from this order have been described. Some of them typified new phylogenetic orders Nodosilineales and Oculatellales. Herein, five ‘Leptolyngbya-like’ CALU strains were described as a separate cluster of Nodosilineales, and assigned to the family Nodosilineaceae. Besides separate 16S rRNA gene phylogeny, this cluster was supported by the analysis of 16S–23S ITS composition, as well as of rpoC1 and rbcL genes phylogeny records. Based on the polyphasic description, a new genus Ingrithrix gen. nov. (Nodosilineaceae, Nodosilineales) with a new species I. praediumpetri represented by five ‘Leptolyngbya-like’ CALU strains was proposed. Taxonomic diagnosis of the genus Ingrithrix was based on phylogenetic distinction from other Nodosilineaceae genera, and phenotypically substantiated by an ability to produce ‘red-shifted’ chlorophylls d and f in dependence on far-red (>700 nm) light, as well as by freshwater habitat and low tolerance to elevated salt concentration. Description of the genus Ingrithrix justified attention to ‘red-shifted’ chlorophylls in cyanobacterial taxonomy, and noticeably increased the availability of test objects with this non-trivial property.