It was first discovered in the Teska member of the Ust'-Pinega formation, in a thick lens of sandstone, originally sand dumped by storm waves that cut a deep channel through the shallow sea bottom where the organisms lived.

However, a nearby site discovered later by Mikhail Fedonkin yielded separate specimens which were beautifully preserved in an upright position and showed the internal anatomy.

[1] Ventogyrus is now believed to have lived on or above the sea floor, an egg-shaped organism made of three modules (like the sections of an orange), all connected to a central rod.

Some follow Dolf Seilacher's theory that Ediacarans including Ventogyrus are an extinct phylum, the Vendobionta, related to no other living things.

Ventogyrus is unusual among organisms proposed as vendobionts because paleontologists have also suggested relationships with post-Ediacaran fossils, including Erytholus from the Cambrian.

[2] Fedonkin has suggested, based on details of internal anatomy, that Ventogyrus could have been the float organism of a siphonophore colony (living examples include the Portuguese Man O' War).

Ivantsov considers it an early representative of the phylum Ctenophora, the comb jellies, an ancient group whose members resemble but are not related to jellyfish.

Ventogyrus does not fall obviously within one of the main form taxa of Ediacarans, the rangeomorphs, the erniettomorphs, and the trilobozoans, but it is also not obviously a member of a known biological taxon.