|“||A boy and his Blade. And still no match for the new Queen. So, first... You'll die... Painfully. And then Crowley will watch his son die -- ditto -- and then the King himself. And Blade destroyed. That's quite a to-do list.||”|
After becoming a demon, Cain created the Knights of Hell on Lucifer's orders, leading the order in creating chaos and darkness across the world for centuries. Eventually, Cain fell in love with a woman named Colette Mullen and left the Knights of Hell to marry her and retire. In response, the Knights kidnapped Colette to force Cain to come back to them. In retaliation, Cain hunted down the Knights of Hell and slaughtered all but Abaddon with the First Blade. When Cain found Abaddon, she was possessing Colette and tricked Cain into killing his wife. Cain left Abaddon alone as Colette's last request was that he stop the killing and not go after Abaddon for revenge.
In 1958, Abaddon resurfaced at St. Bonaventure Convent, running a "demon factory" to steal souls and turn them into demons loyal to her. Henry Winchester and Josie Sands investigated, exorcising two of Abaddon's demons, but Abaddon overpowered them and possessed Josie to infiltrate the Men of Letters without Henry's knowledge. On August 12, 1958, Abaddon slaughtered the Men of Letters on the night of Henry and Josie's initiation. Henry escaped through time, but Abaddon followed him and fought him and his grandsons Sam and Dean Winchester for possession of the Key of the Order of Letters. Abaddon was defeated and imprisoned, but eventually escaped after hearing about how the "salesman" Crowley now ruled Hell. After Crowley had been captured, Abaddon tried to kill him to take control of Hell for herself, but was forced from Josie's body when Sam doused her in Holy Fire.
Shortly after her defeat at Sam's hands, Abaddon had a demon loyal to her perform a ritual to restore Josie's body for her to use as her vessel. Abaddon then began organizing a campaign to overthrow Crowley and take over Hell, planning to go after the humans and angels once she had control of Hell. Crowley was eventually released by the Winchesters after helping to free Sam from possession by Gadreel and started his own campaign against Abaddon to win over the hearts of the minor demons in Hell. To help with his efforts to stop Abaddon, Crowley formed an alliance with the Winchesters and they began seeking out the First Blade to kill Abaddon with. After locating Cain, Dean got the Mark of Cain and a clue to the First Blade's location, but a demon loyal to Abaddon named Lola learned of their hunt for the First Blade and informed Abaddon of it. The Winchesters and Crowley were able to locate and retrieve the First Blade, but Crowley took possession of it until such time as Abaddon could be located so the Winchesters couldn't use it against him. Though annoyed with Dean's obsession over finding Abaddon, Sam eventually joined him after learning of Abaddon's continuing efforts to make a demon army through stealing souls.
Eventually, Abaddon made her move by traveling back in time and kidnapping Crowley's son Gavin in order to have leverage over him. Abaddon takes Gavin to the Humboldt Hotel in Cleveland, Ohio where Crowley is meeting with his trusted advisors about the situation in Hell, not knowing that his advisors have betrayed him to Abaddon. Abaddon tells Crowley she knows that he helped the Winchesters get the Mark of Cain and the First Blade and suggests that they work together to destroy the Winchesters before fighting it out amongst themselves since the Winchesters will likely use the First Blade to kill Crowley after they deal with her. Crowley refuses so Abaddon brings out Gavin, believing that Crowley has enough humanity left in him from his human blood addiction to give in if she tortures his son. Abaddon begins making Gavin's eyes bleed and causes him extreme pain to get to Crowley. Crowley refuses to give in until Abaddon increases Gavin's pain at which point his lingering humanity causes him to agree to help Abaddon as she expected.
After bonding with Gavin for a while, Crowley agrees to help Abaddon kill the Winchesters and calls Dean, telling him he's found Abaddon and will give Dean the location of the First Blade so they can kill her. Crowley sends the Winchesters to St. Anthony's Cemetery where he'd buried the First Blade in a corpse so they can retrieve it, but they are attacked by a hellhound Crowley had left to guard the weapon. Dean calls Crowley who calls off the hellhound and they are able to safely retrieve the First Blade. Dean then calls Crowley back and is told to meet him at the penthouse suite of the Humboldt Hotel where Crowley will draw out Abaddon for Dean to kill her. Before hanging up, Crowley tells him that the hotel is "a good day's drive from Poughkeepsie", a code word Dean had told him in the past he and Sam use to warn each other of a trap. Though Abaddon doesn't pick up on the warning and he doesn't tell Sam, Dean gets that Crowley is warning him that its a trap.
After Crowley lures the Winchesters to the Humboldt Hotel, Abaddon shoots him with a devil's trap bullet to immobilize him, a trick she had learned from Henry Winchester. Abaddon explains that her thinking is that when the Winchesters arrive, she will be facing off with them, the First Blade and potentially Crowley which she sees as stiff odds. Abaddon intends to use the bullet to keep Crowley out of the fight so she can kill the Winchesters and destroy the First Blade.
Arriving at the Humboldt Hotel, Dean sends Sam to the basement with the excuse that Crowley had seen demons going there while he heads to the penthouse to face Abaddon alone. Dean enters the penthouse suite, subtly showing Crowley that he's armed with the First Blade. Crowley promises to take Dean to Abaddon, telling him that its not far and signals Dean to a demon that's about to attack him. Dean quickly kills the demon with the First Blade, but is then pinned to the wall by Abaddon who enters the room. Abaddon is amused by the fact that even armed with the First Blade, Dean is no match for her and tells him that she's going to kill him painfully, followed by Gavin and Crowley before destroying the First Blade. Dean concentrates hard, activating the Mark of Cain which allows him to start fighting through Abaddon's power. Despite Abaddon pushing ever harder against him with her powers, Dean makes slow progress towards her, but Abaddon is eventually able to pin him against the wall again, causing Dean to drop the First Blade. As Abaddon laughs at him, Dean concentrates hard on the First Blade and manages to make it fly into his hand with telekinesis to Abaddon's shock.
As Sam enters the room, having discovered no demons in the basement, Dean drops off the wall, now completely immune to Abaddon's powers. As Abaddon stands stunned at this new development, trying to regain power over Dean, Dean charges Abaddon and stabs her in the stomach with the First Blade, lifting her off the ground as he does. The First Blade causes energy to course through Abaddon, killing her. In a state of rage brought on by the Mark of Cain, Dean starts mutilating Abaddon's corpse, repeatedly attacking it with the First Blade until Sam gets through to him that Abaddon's dead.
Following Abaddon's death, the Winchesters choose to let Crowley go rather than kill him too and he removes Abaddon's bullet with a knife. Though the Winchesters demand he return his son to his own time, Crowley takes off with him for Gavin to start a new life as he will die if he returns to the past. With Abaddon dead, Crowley regains full control of Hell and later executes demons that betrayed him in various ways to Abaddon.
Killing Abaddon pushes Dean further under the influence of the Mark of Cain and he refuses to be parted from the First Blade when Sam suggests it after they leave the Humboldt Hotel. Sam later informs Castiel that Dean killed Abaddon "and then some" to the angel's great worry as both notice that Dean is falling further under the Mark's influence.
- Until Metatron's death while rescuing Lucifer from the Darkness two years later, this battle features the final death of a Big Bad. It is also the final death of a Big Bad in battle with the good guys as Metatron sacrificed himself to buy the Winchesters time to escape with Lucifer.
- Against Abaddon, Dean displays immunity to her powers and telekinesis, both achieved due to the Mark of Cain and great concentration. While he briefly displays telekinesis to retrieve the First Blade against Metatron, he never shows immunity to demonic powers again while wielding the Mark of Cain.
- Abaddon shoots Crowley with a devil's trap bullet to keep him from interfering in her fight with Dean. This is the same way Dean and Henry defeated her the first time. She credits Henry for the idea when telling Crowley what she was doing.
- Crowley warns Dean of the trap using the word Poughkeepsie. Dean had told Crowley that Poughkeepsie was a code word he and Sam use to warn each other of traps when Crowley helped him save Sam from Gadreel in Road Trip.
- When Dean kills Abaddon's minion during the battle, he has the same glow as any demon Dean's ever killed with the demon-killing knife despite Dean using the First Blade. However, when Dean kills Abaddon, she dies in a similar manner to when an angel or Cain smites a demon.