As recorded at Genesis 3:14, Jehovah God addressed the serpent that had deceived Eve in the garden of Eden. God said: “Because you have done this thing, you are the cursed one out of all the domestic animals and out of all the wild beasts of the field. Upon your belly you will go and dust is what you will eat all the days of your life.” The Bible does not specifically state that the animal used in tempting Eve had previously had legs but lost them. While the wording of Genesis 3:14 might lead some to think so, we need not necessarily conclude that prior to this curse, serpents had legs. Why not?

Principally because the real object of Jehovah’s judgment was Satan—the invisible spirit who had misused that lowly animal. The Bible describes Satan as “the father of the lie” and “the original serpent.” Both of these expressions apparently point back to Satan’s using a visible animal, a serpent, as his mouthpiece to induce Eve to disobey God’s command.—John 8:44; Revelation 20:2.

God created serpents, and Adam had apparently given serpents their name before Satan’s deceptive act. The unreasoning serpent that spoke to Eve was not to blame. It would have been unaware that Satan was manipulating it, and it could not understand the judgment that God rendered against the disobedient parties.

Why, then, did God speak of the serpent’s physical abasement? The behavior of a serpent in its natural environment, crawling on its belly and flicking its tongue as if to lick up dust, fittingly symbolized Satan’s debased condition. Having previously enjoyed a lofty position as one of God’s angels, he was consigned to the lowly condition referred to in the Bible as Tartarus.—2 Peter 2:4.

Further, as a literal serpent might wound a man’s heel, Satan in his debased state would ‘bruise the heel’ of God’s “seed.” (Genesis 3:15) The primary part of that seed proved to be Jesus Christ, who temporarily suffered at the hands of Satan’s agents. But the symbolic serpent’s head will, in time, be permanently crushed by Christ and his resurrected anointed Christian companions. (Romans 16:20) Thus, God’s directing his curse toward the visible serpent aptly pictured the debasement and ultimate destruction of the invisible “original serpent,” Satan the Devil.

My comments: This serpent was likely perched in a tree at the time, and may have been arboreal. Thus, after the command to slither on its belly and to eat dust was given, it was likely observed by the couple to do just that, to leave its branch, slither down the trunk, and then slither away on the ground with its tongue flashing in and out as it went. But this was an illustration of Satan’s debasement. The exoteric serpent was illustrative of the esoteric serpent Satan.

There are however two other scriptural uses of the serpent eating dust. These being Isaiah 65:25 and Micah 7:17, considered in turn below:

The final verse of Isaiah 65 declares: “The wolf and the lamb themselves will feed as one, and the lion will eat straw just like the bull; and as for the serpent, his food will be dust. They will do no harm nor cause any ruin in all my holy mountain,” Jehovah has said.” (Isaiah 65:25) This promise was first meant for the Jews returning home from the Babylonian exile. Thus, its original application assured them that they had nothing to fear from wild animals during their restoration project. The wolves would not hunt their lambs, the lions would not hunt their livestock, and the serpents would not attack them. For them, Isaiah 65:25 would be effectual not literal. (Effectual in that the wolves and lions would not literally be vegetarian, and the serpent would not abandon predation. It would only seem that way to them, as far as they were concerned.) The Isaianic serpent ingesting dust is therefore separate from the “curse” of the Edenic serpent.