When local newspapers report strange things seen floating in rivers during a historic flood in Vermont, Wilmarth becomes embroiled in a controversy regarding the reality and significance of the sightings.

Wilmarth explains the understanding of some of Akeley's letters about the cosmology of reality as he learned, stating: Even now I absolutely refuse to believe what he implied about the constitution of ultimate infinity, the juxtaposition of dimensions, and the frightful position of our known cosmos of space and time in the unending chain of linked cosmos-atoms which makes up the immediate super-cosmos of curves, angles, and material and semi-material electronic organisation.As the story concludes, Wilmarth discloses the discovery from which he fled in terror: Akeley's discarded face and hands.

He now believes with a dreadful certainty that the cylinder in that dark room with that whispering creature already contained the brain of Henry Wentworth Akeley.

"[3] Wilmarth is the main character in Fritz Leiber's "To Arkham and the Stars", written and presumably set in 1966, when the now-septuagenarian professor is chair of Miskatonic's Literature Department.

"[5] Wilmarth remarks in the story, "[A]fter you've spent an adult lifetime at Miskatonic, you discover you've developed a rather different understanding from the herd's of the distinction between the imaginary and the real.

The 1976 Fritz Leiber story "The Terror From the Depths" mentions Akeley being consulted at his San Diego home by Professor Albert Wilmarth in 1937.

During his jaunt, he met a local farmer with a name that bears a striking resemblance to the ill-fated character of Lovecraft's tale: one Bert G.

The following passage from The Whisperer in Darkness lists the names of various beings and places that occur in the works of Lovecraft and other writers: I found myself faced by names and terms that I had heard elsewhere in the most hideous of connections—Yuggoth, Great Cthulhu, Tsathoggua, Yog-Sothoth, R'lyeh, Nyarlathotep, Azathoth, Hastur, Yian, Leng, the Lake of Hali, Bethmoora, the Yellow Sign, L’mur-Kathulos, Bran, and the Magnum Innominandum…Among the more obscure names mentioned here are: In "The Whisperer in Darkness", narrator Albert Wilmarth initially dismisses those who believe that nonhuman creatures inhabit the Vermont hills as "merely romanticists who insisted on trying to transfer to real life the fantastic lore of lurking 'little people' made popular by the magnificent horror-fiction of Arthur Machen.

In both cases we have a professor, an antiquarian, following his avocational interests in what most would dismiss as superstition on a dangerous expedition into a strange region of ominous domed hills.

[21] As noted by critics like Price and Lin Carter,[22] The Whisperer in Darkness also makes reference to names and concepts in Robert W. Chambers's The King in Yellow, some of which had previously been borrowed from Ambrose Bierce.

In a letter to Clark Ashton Smith, Lovecraft wrote that "Chambers must have been impressed with 'An Inhabitant of Carcosa' & 'Haita the Shepherd', which were first published during his youth.

But he even improves on Bierce in creating a shuddering background of horror—a vague, disquieting memory which makes one reluctant to use the faculty of recollection too vigorously.

The idea of keeping a human brain alive in a jar (with mechanical attachments allowing sight, hearing, and speech) to enable travel in areas inhospitable to the body might have been inspired by the book The World, the Flesh, and the Devil by J. D. Bernal, which describes and suggests the feasibility of a similar device.

In addition to being a textbook example of Lovecraft's characteristically non-occult brand of horror, in an age when the genre consisted almost entirely of ghosts, vampires, goblins, and similar traditional tales, "Whisperer" is one of the earliest literary appearances of the now-cliché concept of an isolated brain (although the alien brain case is not transparent as with later cinematic examples of this trope).

The story retains some seemingly supernatural elements, such as its claim that the alien fungi, although visible to the naked eye and physically tangible, do not register on photographic plates and instead produce an image of the background absent the creature (an impossibility by any known laws of optics, though a trait commonly attributed to vampires), although the story does mention that this is possibly due to the creatures' fungoid and alien structure which works differently from any known physical organism.

It is stated that the electrons of these fungoid aliens possess a different vibrational frequency that would require the development of a novel technique by a chemist in order to record their image.

In a letter to the January 1932 Weird Tales, Donald Wandrei praised The Whisperer in Darkness, as well as "The Seeds of Death" by David H. Keller and the stories of Clark Ashton Smith.

However, Weinberg also praised "the detailed buildup" of The Whisperer in Darkness, arguing it created "the superb mood that needed no surprise to make it a classic of fantastic horror".