The serpent’s conversation with Eve in Genesis 3 offers a unique window into how readers throughout history have approached interpreting the text. This relatively brief narrative of a snake speaking to a human in the Garden of Eden has prompted centuries of thought on what the text means and how it should be understood. The interpretive history of this passage reveals that even what might seem like straightforward readings of the text are shaped by the interpreter’s understanding of nature, history, and their own cultural context.
Early Jewish interpreters often approached the speaking serpent through a remarkably literal lens. Many texts from the early Second Temple period and after present a world where the snake’s ability to speak required no special explanation and simply reflected the original, natural state of creation. These interpreters envisioned Eden as a place where all animals possessed language and could communicate with humans in a common tongue. This reading treated the serpent’s speech not as a supernatural intrusion, symbolism, or literary device, but as a natural feature of the original state of the world. The loss of animal speech then became a part of all of the changes that came following humanity’s disobedience, transforming the world from its original design.
While there are supernatural interpretive traditions of the serpent that find connections between the Hebrew term ‘nachash’ as a possible reference to a divine being in the garden, most of the earliest recorded interpretive tendencies were focused on an almost hyper-literal, naturalistic reading. These interpreters didn’t explain away the snake’s speech as a literary device or identify it with supernatural forces. Instead, they leaned on what they felt was the most literal reading, creating detailed accounts of how and why animals could simply speak and then lost that ability to speak. This interpretive trajectory demonstrates how readers in every era, even operating under what they perceived as the most straightforward reading, bring their own assumptions about the world to their understanding of scripture, shaping what counts as a ‘plain’ or ‘normal’ reading of the text.
Now the serpent was shrewder than any of the wild animals that the Lord God had made. He said to the woman, “Is it really true that God said, ‘You must not eat from any tree of the orchard’?” The woman said to the serpent, “We may eat of the fruit from the trees of the orchard; but concerning the fruit of the tree that is in the middle of the orchard God said, ‘You must not eat from it, and you must not touch it, or else you will die.’” (Genesis 3:1-3)
On that day, as he was leaving the Garden of Eden, he burned incense as a pleasing fragrance — frankincense, galbanum, stacte, and aromatic spices — in the early morning when the sun rose at the time when he covered his shame. On that day the mouths of all the animals, the cattle, the birds, everything that walks and everything that moves about were made incapable of speaking because all of them used to converse with one another in one language and one tongue. He dismissed from the Garden of Eden all the animate beings that were in the Garden of Eden. All animate beings were dispersed — each by its kind and each by its nature — into the places which had been created for them. But of all the animals and cattle he permitted Adam alone to cover his shame. (Jubilees 3:27-30)
The book of Jubilees, an early Second Temple period retelling of Genesis and Exodus, exemplifies this literal approach by matter-of-factly explaining that the serpent could speak because all the animals could speak. According to this text, on the very day Adam left the Garden, all the animals, cattle, birds, everything that walked or moved, lost that ability, and prior to this moment, Jubilees presents a world where all creatures conversed with one another in a single, shared language. The serpent’s conversation with Eve is just another instance of this phenomenon; it simply reflects what the author thought was the normal state of creation before the expulsion from the garden.1
Jubilees treats this transformation as parallel to humanity’s own punishment and exile. Just as Adam and Eve are expelled, so too are all the animals dismissed from Eden and dispersed to their new habitats throughout the earth. The loss of speech becomes part of the overall change in the condition of creation, while humanity retains language but must now labor and suffer, animals lose their rationality and communicative abilities entirely. The text presents this not as metaphor or allegory but as a simple historical fact, part of the reshaping of the world after the first sin. In Jubilees’ telling, the emphasis remained on a ‘literal’ reading in light of how they viewed the order of the world.
... when he saw that the disposition of man had a tendency to wickedness, and was but little inclined to holiness or piety, by which qualities an immortal life is secured, he drove them forth as was very natural, and banished him from paradise; giving no hope of any subsequent restoration to his soul which had sinned in such a desperate and irremediable manner. Since even the opportunity of deceit was blameable in no slight degree, which I must not pass over in this place. It is said that the old poisonous and earthborn reptile, the serpent, uttered the voice of a man. And he on one occasion coming to the wife of the first created man, reproached her with her slowness and her excessive prudence, because she delayed and hesitated to gather the fruit which was completely beautiful to look at, and exceedingly sweet to enjoy, and was, moreover, most useful as being a means by which men might be able to distinguish between good an evil. (Philo, On the Creation)2
Philo of Alexandria, writing from within a Hellenistic Jewish context, offers a similarly plain reading here in On the Creation. While Philo is well known for his allegorical interpretations of scripture, and elsewhere does offer allegorical readings of Genesis and the serpent, his treatment of the serpent here specifically takes a relatively straightforward approach.3 He describes the serpent unambiguously as an ‘earthborn’ reptile that possessed a human voice and came to speak with Eve about the fruit of knowledge. Like Jubilees, Philo presents this ability as requiring no special explanation; the serpent simply had the capacity for speech.
Where Jubilees provides a more elaborate description of how all the animals lost their speech as part of the punishment and expulsion from the garden, Philo concentrates on the serpent’s role in the deception itself. He emphasizes the serpent’s cunning approach to Eve, describing how it reproached her for hesitating to take the fruit that appeared beautiful and promised the ability to distinguish good from evil. Philo doesn’t elaborate on what happened to animal speech afterward or describe a universal transformation like Jubilees does. Rather, his concern lies more with the moral and theological implications of the deception than with constructing a comprehensive account of how the world changed. Still, even under his usual layers of allegory, lies an assumption about how the natural world operated and what a straightforward reading of the narrative includes.
Now the snake was the wisest of all the wild animals that were upon the earth, which the Lord God had made. And the snake said to the woman, “Why is it that God said, ‘You shall not eat from any tree that is in the orchard’?” And the woman said to the snake, “We shall eat of the fruit of the tree of the orchard, but of the fruit of the tree that is in the middle of the orchard, God said, ‘You shall not eat of it nor shall you even touch it, lest you die.’” (LXX Genesis 3:1-3)4
The Greek translation of Genesis 3 in the Septuagint, a translation in use throughout Hellenistic Judaism by the time of Philo, provides additional evidence for this naturalistic understanding of the serpent. In its rendering of Genesis 3, this text presents the snake explicitly as one among many animals, emphasizes the serpent’s place within the created order of animals and using generic terminology for snakes rather than any specialized or supernatural designation.5 Significantly, where the Hebrew text might leave some ambiguity about who is speaking, the Septuagint repeatedly clarifies that it is indeed the serpent that speaks to the woman, reinforcing the straightforward reading that this is an animal with the ability to speak, with no further explanation.
The choices made in the creation of the Septuagint suggest that its translators, similarly to Philo, assumed a background where animal speech in Eden was unremarkable. The Greek renders the Hebrew description of the serpent with the word meaning ‘wise’ or ‘prudent’, a term with generally positive connotations rather than the more ambiguous or negative implications of the Hebrew ‘shrewd’. This choice presents the serpent as the wisest among all the animals, maintaining its status as an animal among animals while acknowledging its particular intelligence. The translators apparently felt no need to otherwise address how a serpent could speak or to distance themselves from the literal sense of the narrative. The translation thus coheres with the contemporary interpretive traditions represented by Jubilees and Philo, treating the speaking serpent as a part of the natural order.
God therefore commanded that Adam and his wife could eat from all the rest of the plants, but should avoid the Tree of Knowledge; and foretold that if they touched it, it would lead to their destruction. But while all the living creatures had one language at that time, the serpent, which then lived together with Adam and his wife, showed an envious disposition at his assumption of their living happily and in obedience to God’s commands. And thinking that if they disobeyed them, they would fall into misery, he persuaded the woman, out of a malicious intention, to taste of the Tree of Knowledge, telling them that in that tree was the Knowledge of Good and Evil; and that when they obtained it, they would lead a happy life, indeed a life not inferior to that of a God. (Josephus, Antiquities of the Jews)6
Josephus, the first-century Jewish historian who was writing contemporaneously with the New Testament, was himself likely influenced by his use of the Septuagint. In his retelling of the Eden narrative, Josephus states directly that all living creatures possessed one language at that time, echoing the same directness as in Jubilees. The serpent appears in his account as a creature that lived alongside Adam and his wife in the Garden, not as an intruder or supernatural being, but as part of the original community of Eden. Josephus describes the serpent’s motivation in entirely naturalistic, if human-like, terms in that it felt envy, leading it to persuade the woman to eat from the tree.
Unlike the Hebrew text’s ambiguous or negative characterization of the serpent, Josephus makes no mention of special cunning or shrewdness, likely following the Septuagint’s more positive rendering of the serpent as ‘wise’.7 His matter-of-fact presentation assumes readers will accept without question that a serpent could speak, feel envy, and devise plans, because this was simply the nature of animals in the beginning. Josephus thus serves as an additional witness to this interpretive tradition. Writing in Greek for a broader audience beyond the Jewish community, he nevertheless maintains the thoroughly literal reading that treats the serpent’s speech as historical fact, requiring explanation only in terms of what all animals could do before the world was transformed by human sin.
These early interpretations of Genesis 3 reveal an insight about biblical reading, namely that what qualifies as a ‘literal’ interpretation is itself still shaped by the interpreter’s cultural context and worldview. For readers in the Second Temple period, a straightforward, historical reading of Genesis seems to have consistently included talking animals as a normal feature of the early state of creation. Their literal sense of the text expanded to encompass details that many modern readers would likely feel forced to consider fantastical or symbolic. This difference demonstrates that even the most earnest attempt to read scripture ‘as written’ inevitably filters the text through assumptions about nature, history, and possibility that vary across times and cultures. The history of the serpent in interpretive history thus offers more than insight into a particular passage; it reveals how the very category of ‘literal’ readings shift along with the readers who employ it.
Wells, A. Rahel ‘One Language and One Tongue’: Animal Speech in Jubilees 3:27–31 (pp. 319-337) Journal for the Study of the Pseudepigrapha, Vol. 28, No. 4, 2019
Fischel, Henry Albert Rabbinic Literature and Greco-Roman Philosophy: A Study of Epicurea and Rhetorica in Early Midrashic Writings (pp. 29-30) Brill, 1973
Brodt, Brenda The Serpent’s Identity in Genesis 3: A History of Jewish Interpretation from the Bible Through the Thirteenth Century (p. 19) McGill University, 2002
Brodt, Brenda The Serpent’s Identity in Genesis 3: A History of Jewish Interpretation from the Bible Through the Thirteenth Century (pp. 22-23) McGill University, 2002
Nice piece. Just a small note regarding the date of the Septuagint, you put it as contemporaneous to philo, when the Septuagint (at least on the pentateuch) was translated at least two centuries before probably as early as the 3rd century bce.
It might be interesting to point out that many medieval Jewish commentators (such as Ibn Ezra) also emphasize that a literalist reading should be adopted here, but for them it shows that the snake alone, not all animals, possessed human language. This is due to its status as the "the shrewdest of all animals" as attested to in Gen 3:1.
This has more in common with common Christian interpretations associating the snake with Satan, although it still maintains a strictly literalist reading. (I would argue that this was indeed the original understanding as well.)