The fungus produces small white mushrooms with caps up to 9 mm (0.35 in) in diameter, supported by thin stems that originate from a yellowish-brown sclerotium.

The mushroom is difficult to distinguish from the other two species of Collybia unless an effort is made to examine the sclerotia, which is usually buried in the substrate.

[3] In a 1935 publication, Jean D. Arnold reported a series of cultural studies with monokaryon isolates (hypha having only a single haploid nucleus) of several Collybia species to determine their mating type.

This sexual incompatibility indicated that the two taxa were separate species, and she raised the taxon from varietal to specific status, calling it Collybia cookei.

[7] A 2001 molecular analysis based on the ribosomal DNA sequences confirmed that C. cookei is phylogenetically related to C. tuberosa and C. cirrhata, and that the three species form a monophyletic group that comprise the genus Collybia.

[9] The upper region of the stem surface can be covered with what appears to be a white powder, and there are thin hairs near the base.

[11] Using a microscope provides a more definitive way of distinguishing the two: the hyphae in the sclerotia of C. cookei are rounded, while those of C. tuberosa are elongated; this diagnostic character is apparent with both fresh and dried material of the two species.

[10] Another mushroom that grows on decomposing fruit bodies is Asterophora lycoperdoides, which is distinct from C. cookei because of the powdery brown asexual spores (chlamydospores) produced on the cap surface.

[14] Alexander H. Smith has noted a general similarity in appearance between C. cookei and the North American species Clitocybe sclerotoidea (then known as Tricholoma sclerotoideum),[15] which is parasitic to Helvella lacunosa.

[15] Like all members of the genus Collybia, C. cookei grows on the well-rotted, blackened remains of mushrooms, such as species of Russula,[9] Meripilus giganteus,[17] and Inonotus hispidus.