Why Is Satan a Talking Serpent in Genesis 3?

Let’s get a few housekeeping matters out of the way first:
(1) I believe Genesis 3 is a true historical account about real conversations that took place between real characters in a real place.  I don’t think the account is mythical or metaphorical for some unapparent meaning.
(2) The serpent is clearly identified as Satan in places like Rev 12:9 and 20:2.
(3) Serpents, like the rest of non-human creatures, don’t possess verbal skills of speech communication.
(4) In passages like Job 1 and Zechariah 3, Satan apparently remains in his angelic form, so there’s no reason to think a serpentine manifestation is necessary for him to do his serpentine work.

Now to the question at hand: why do we see a talking serpent in Genesis 3?

Beasts Were Under Dominion
The wording of Genesis 3:1 starts us in the right direction: “Now the serpent was more crafty than any other beast of the field that the LORD God had made.”  Beasts, according to 1:26 and 1:28, were to be ruled by God’s image-bearers.  God did not make animals to rule and subdue the earth; he made man for that.  Man would exercise dominion over the beasts, in particular “every creeping thing that creeps on the earth” (1:26).  The serpent, like all other creatures, was under the dominion of Adam and Eve.

What you see happening in Genesis 3 is the subversion of God’s created order. The serpent exercises dominion over the woman with his deceptive words.  This is a reversal of God’s design, and Satan knows it.  He wants to turn the whole thing upside down.

Subversion At Every Level
Consider the bigger picture of what’s happening.  God commanded Adam to not eat from the tree of the knowledge of good and evil (Gen 2:16-17), and Adam apparently conveyed that command to Eve who referenced it in her conversation with the serpent (3:2-3).  So Adam and Eve, God’s image-bearers, should’ve listened to their Creator, but they didn’t.  Adam shouldn’t have listened to the voice of his deceived wife, but he did (3:17).  Adam and Eve should’ve subdued the crafty serpent, but they didn’t.

Genesis 3 is a story of subversion at every level: a creature prevails over the image-bearers who fail in their responsibilities both to one another and to God.  If Satan deceived Eve while in angelic form, that appearance may’ve still been effective, for interaction with a heavenly being might lower defenses.  Rather than only inserting the knife, Satan as a serpent rules over God’s rulers and sets the snare for their failure and fall.  The fact that Eve believed the lies of a serpent meant the knife went in deep and with a painful twist.

Probably, then, Satan comes to Eve as a serpent in order to subvert God’s design at every level.  The image-bearers defy their Creator as a creature exercises dominion over them.

Shape-Shifting? Ventriloquism? Possession?
What is the relationship between Satan and the serpent?  This is not an easy question, but I see three possibilities.

First, did Satan simply shape-shift into the serpent and later return to his angelic form?  There’s no precedent for angels doing this sort of thing in Scripture, so I don’t consider this the probable explanation.

Second, did Satan somehow independently animate the serpent to speak, sort of like a ventriloquist who takes a dummy and makes it do what it cannot innately do?  Maybe.  Scripture records one other talking animal, Balaam’s donkey, but that animal speaks because of God’s enablement (Num 22:28).  Perhaps Satan could use his own power to accomplish such an act.

Third, did Satan possess the creature?  I find this explanation most compelling.  According to the Bible, demons can possess people, and even Satan did so with the example of Judas.  But in Mark 5:1-13, Jesus encounters a demon-possessed man whose demons (known collectively there by the name “Legion”) beg to go into a herd of pigs. “Send us to the pigs; let us enter them,” they pleaded with Jesus (5:12).  Jesus permitted this animal possession, so the demons possessed the herd and rushed down into the sea (5:13).

So what can we say about the relationship between Satan and the serpent?  Animals can be supernaturally enabled to talk (e.g. the serpent in Gen 3 and Balaam’s donkey in Num 22), demons can talk through the one possessed (e.g. the Legion who speak through the man in Mark 5), and they can even possess animals (e.g. the herd in Mark 5).  Using later Scripture to inform our reading of Genesis 3, then, I think the best explanation of the talking serpent is that it is a creature possessed by Satan himself.


I welcome any interaction on the above points.  Do you find my explanation convincing, or is there a different explanation you believe is more reasonable?


3 thoughts on “Why Is Satan a Talking Serpent in Genesis 3?

  1. Mitch, this idea of subversion in Genesis 3 may find a parallel in Genesis 6:1-4 as a repetition of the fall. Man is multiplying, though through the subversion of God’s design. The sons of God saw something attractive and ‘good’ and took it. If Jude 6 is describing Genesis 6, it confirms subversion as the root sin of this other odd fall account. “The angels did not stay within their own position of authority, but left their proper dwelling, ….” Maybe both Gen 3 and Gen 6 are pointing to the uncreation of the fall through unholy subversion?

  2. If the serpent is only possessed by Satan then why is the serpent cursed, it is only a creature that was allegedly hijacked by Satan. Also, the serpent in Genesis was at least walking on 4 legs if not on 2 legs and then was cursed to from then on go on its belly and be hated by people. The serpent of Genesis is in fact an intelligent ancient reptilian being who was soomeplace he was not supposed to be (the garden of eden).

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