|“||The Mark and the Blade work together. Without the Mark, the Blade is useless. It's just an old bone.||”|
Since the Mark of Cain has been destroyed, the blade is now rendered useless and powerless.
When Cain realized that his brother Abel was talking to Lucifer, and not God, Cain offered an exchange where his younger brother would go to Heaven and Cain would take his place in Hell. Lucifer agreed, on the condition that Cain himself would send his brother to Heaven. Cain then fashioned a weapon out of the jawbone of a donkey and used it to kill his brother.
Lucifer transferred the mark to Cain, which somehow linked its power with the blade. This made the First Blade, when held by the bearer of the mark, powerful enough to kill anything. However, without the mark, the blade would simply be a bone.
1863EditCain has since retired from his job, having met his wife Colette, who forgave him despite his deeds. However, this angered the Knights of Hell, leading Cain to destroy his very creations. In Jasper Springs, Mississippi, he hunted demons protecting the last remaining knight. To his shock, he found out that Abaddon had possessed Colette. Abaddon threatened to kill Colette if Cain did not return to his job as a knight. Cain refused and stabbed his wife with the First Blade, but not before Abaddon left Colette's body.
At this time, Cain made a promise to Colette that he would no longer work as a Knight. Since nothing could destroy the First Blade, Cain threw it into the bottom of the deepest ocean during his retirement, so that he would be able to keep his promise.
The First Blade was being located by Crowley in order to give it to its new owner, Dean, who also has been given the Mark of Cain. The two want it to kill Abaddon as it is the only weapon that can kill a Knight of Hell. Before "falling off the wagon," Crowley learned that the Blade was picked up from the bottom of the Marianas Trench by an unmanned submarine and passed among various people. Eventually Sam, Dean and Crowley track it down to rogue Man of Letters Magnus who took the Blade to add it to his vast collection of artifacts. After Magnus tries to add Dean to the collection, Dean is forced to decapitate Magnus with the Blade to save Sam, but it has a negative effect on him when he holds it. Not trusting Sam and Dean, Crowley steals the Blade until Sam and Dean can find Abaddon.
Crowley later reveals where he hid it in a corpse in a grave and Sam and Dean retrieve the Blade. Dean uses it to kill a demon then face against Abaddon herself. With the power of the Mark of Cain, Dean eventually proves immune to Abaddon's powers and uses telekinesis to retrieve the Blade when he loses it. Dean stabs Abaddon in the stomach with the First Blade, killing her in a massive burst of red light. He then stabs her corpse several times with the Blade before stopping. With Abaddon dead, Sam suggests getting rid of the Blade due to the effect it has on Dean, but he refuses.
When Dean attempts to use the First Blade to interrogate the reaper Tessa, she promptly impales herself on the Blade, telling Dean "Thank you." Tessa had become suicidal over hearing the voices of trapped souls in the Veil who were unable to get into Heaven because of Metatron's spell.
Gadreel later arrived at the Bunker looking to join with the Winchesters and Castiel in taking down Metatron. Dean approached him to shake his hand, when he suddenly instead removes the First Blade from his jacket and slashes it across Gadreel's chest. Prompting Sam and Castiel to jump on Dean and hold him back as he consumed by bloodlust.
As Dean begins to feel ill, he summons Crowley, who tells him that his sickness is a side effect from the Mark and First Blade. The more he kills the better he will feel, the less he kills the worse he will feel, which will eventually lead to his death as a human was never meant to wield that much power. Dean then has Crowley help him get the First Blade back and escape from the Bunker. Sam later tracks Dean down and the two agree to take down Metatron together. However, after getting the First Blade from the trunk of the Impala, Dean knocks Sam unconscious telling him killing Metatron is something he needs to do alone. Dean confronts Metatron blaming him for everything bad that has happened in the last year. A fight ensues between the two, where Dean is severely beaten by Metatron, and drops the First Blade. Just as he uses his telekinesis to get the First Blade back in his hand, Metatron stabs him in the chest with his angel sword. Sam tries desperately to get Dean help, however Dean dies in Sam's arms.
Sam attempts to summon Crowley to fix the mess he caused, however Crowley is already in Dean's room and begins speaking to Dean's dead body. He tells him that he didn't know the full extent of the Mark of Cain and how Cain too did not like what was happening to him, and tried to kill himself, however his suicide failed, because the Mark wouldn't let him die. Crowley then places the First Blade into Dean's hand, and tells him to wake up. At which point, Dean does being reborn a demon.
While on the run with Crowley, Dean uses the Blade to kill a demon on camera at a gas station in Wisconsin. He also uses it with one of Abaddon's loyalists in an alley behind the bar he was staying at.
Crowley then sends Dean to kill Lester Morris' wife, whose husband sold his soul to have her murdered when she cheated on him. Dean instead decided that Lester was more worthy of death and uses the blade to stab him, after he discovered Lester cheated first. Dean later gets into a fight with a man named Cole, and when he is caught off guard Sam is able to subdue him. As a part of the deal Sam made with Crowley for Dean's location, he hands over the First Blade. Crowley assures Sam that he will either throw the First Blade in a volcano, or leave it on the moon, whatever method of disposal he chooses, he assures Sam that the Blade will be out of Dean's reach.
In The Hunter Games, Metatron reveals that the First Blade is necessary to remove the Mark of Cain so Sam and Dean contact Crowley to get it back. Crowley reluctantly reveals that it is in a crypt in Guam with his bones and agrees to retrieve it. However, Rowena tricks Guthrie into getting it for her before killing him, but Crowley catches her. Rowena tricks Crowley into doubting the Winchesters and he only agrees to give it to them when they have the rest of the spell to remove the Mark.
In The Executioner's Song, Dean calls Crowley for the First Blade after learning that Cain is back to his old ways and needs to be killed. Crowley hands over the First Blade after Cain is stuck in a devil's trap on the condition that Dean return it to him after killing Cain. Dean and Cain fight, but even with the First Blade and Cain trapped in a devil's trap, Dean is no match for the Father of Murder. Cain gets the First Blade back and goes to kill Dean with it, but Dean uses Cain's own knife to cut off his hand, defeating him. After Cain refuses to give up killing, Dean kills him with the First Blade. Afterwards, rather than give it to Crowley as promised, Dean gives it to Castiel who hides it somewhere.
- The true source of the mark, is darkness, whose mark enables the bearer of it to use this weapon to literally kill anything, even God, due to the darkness being stronger than him.
- It has additional effects on the wielder, such as telekinesis, immunity, and super strength, as long as the wielder gives into the Mark's temptation to kill. According to Cain, nothing can destroy the blade but, Abaddon stated that she would destroy the Blade after killing Dean, Gavin and Crowley.
- According to VFX I/O Coordinator, Adam Williams, a quick shot was made to show how the First Blade activated the Mark of Cain once more and brought Dean back to life as a Demon which didn't make the final cut.
- While when killing a normal demon, the Blade causes a glow similar to the Demon-killing knife or the Colt, when killing a Knight of Hell it causes a massive burst of orange/red light to emerge from the Knight's vessel, similar to Cain's smiting ability, and the glow of an angel's vessel when he dies.
- The First Blade, The Colt, the Demon-Killing Knife, Death's Scythe, Angel Blades and Archangel Blades are all legendary weapons that can kill powerful supernatural beings, as well as all being in the brothers' possession at least one point in the series. Each of these weapons has been used at least once by Dean Winchester to kill a powerful being.
- Cain indicated that if he killed Dean with the First Blade, he wouldn't come back.
- When Cain got the First Blade back from Dean, the veins in his arm near his right hand suddenly started becoming pronounced when a close-up shot of Cain's hand holding the Blade is shown.
- The First Blade is the second bone weapon to appear on the show, following the Bone of Righteous Mortal Washed in the Three Bloods of Fallen.
- The First Blade is similar to the Colt, in the way that they both are legendary weapons that is believed to be able to kill any being in the series. And they both require two components to be effective. The Colt requires itself and special bullets, and the First Blade needs the wielder to possess the Mark of Cain.
- Cain, as the creator of the First Blade, was the first to kill with it. He also ended up being the last to be killed by it.