On August 12, 1958, the Knight of Hell Abaddon massacred the Men of Letters. She followed surviving initiate Henry Winchester through time, battling him and his grandsons Sam and Dean Winchester for possession of the Key of the Order of Letters. Abaddon was eventually defeated and imprisoned at the cost of Henry's life. Months later, needing a demon for the Third Trial to close the Gates of Hell, the Winchesters put Abaddon back together to cure her for the Trial. While they are talking to Abaddon, Crowley calls and Abaddon is shocked to learn that Crowley is now the King of Hell as she'd only known him as a salesman. While the Winchesters are distracted with Crowley's phone call, Abaddon manages to escape and returns after the Winchesters have captured Crowley to kill him and take control of Hell for herself. Sam manages to douse Abaddon in Holy Fire, forcing her to abandon her vessel Josie Sands and flee the scene in her smoke form.
A few days after her defeat, Abaddon has a demon loyal to her named Jason perform a ritual to restore Josie's body for her to use as a vessel. Abaddon then gathers together Jason and three other demons to demand to know what's happened to Hell while she's been away as the demons are following Crowley who, to Abaddon, is just a salesman. Abaddon informs the assembled demons that she intends to take control of Hell for herself and lead the demons across the Earth until the humans and angels either bow to her or burn. When a Crossroad Demon shows disbelief in Abaddon's plan and her claim that Crowley is dead, Abaddon exorcises her as punishment and to warn the other demons in Hell that Abaddon is coming.
As her first act towards taking over Hell, Abaddon has Jason and the other two demons possess soldiers to gain better vessels to fight with. Noticing the demon omens their presence caused, the Winchesters investigate the scene and discover the dead vessels. As they realize the demons are now possessing the soldiers, Sergeant Miranda Bates of the Military Police shows them security camera footage revealing Abaddon to be behind what happened to their surprise.
Having gotten the better vessels, Abaddon abducts hunter Irv Franklin and tortures him, causing him to give up Pete and Tracy Bell who are also hunters. Abaddon then tortures Pete and eventually kills him in order to locate the Winchesters so she can find and kill Crowley. Abaddon is able to get one of Dean's phone numbers out of Pete before she kills him and then calls it, getting Kevin Tran. Abaddon passes a message to Kevin to tell the Winchesters that she has Tracy and Irv and will kill them if the Winchesters don't come to save the two. Abaddon also gives Kevin the coordinates of Eugene, Oregon where she is holding Irv and Tracy. Even though the Winchesters know its a trap, they decide to go anyway and order Kevin to find out anything the Men of Letters have on the Knights of Hell, particularly how to kill one.
Sam and Dean make their way to the diner in Eugene, Oregon where Irv and Tracy are still tied up and free the two after checking them for possession with holy water. Knowing that Abaddon and her demons will be coming for them, the four prepare for the fight, arming themselves with holy water, bullets carved with a devil's trap, the demon-killing knife and an angel blade. However, when Sam spots Abaddon's demons coming, they learn that the demons are better armed with assault rifles.
To draw the demons into a trap, Dean records a message on his phone going "come and get it, you dicks" which Jason and another demon follow into the diner. Dean splits them into two teams made up initially of himself and Irv and Sam and Tracy, but switches Irv and Tracy when he learns that Tracy has a problem with Sam due to her family being killed during the Apocalypse. As they prepare to assault the diner and the demons still inside, Irv tells Sam to give him the demon-killing knife while the Winchesters and Tracy flee. Irv explains that Abaddon captured and tortured him until he gave Pete and Tracy up and now he wants to make up for it by sacrificing himself to save the other three. Before the argument can go any further however, Irv is shot through the heart and killed by the third possessed soldier with a sniper rifle, causing Sam to flee into the diner where he's confronted by Jason and the other demon.
As Sam engages the demons after Irv's death, Abaddon attacks Dean and Tracy herself. After Abaddon knocks Dean down, Tracy shoots her with devil's trap bullets, but Abaddon is protected by a bulletproof vest. Dean hits her in the face with holy water and has Tracy run to retrieve the Impala and more weapons while Abaddon is distracted. Dean engages Abaddon one-on-one, drawing an angel blade, but Abaddon easily disarms and overpowers him. Abaddon demands that Dean hand over Crowley to her, promising to kill him quickly if he does. Abaddon warns that if Dean doesn't, she will remove his anti-possession tattoo and take him as her vessel, seeing Dean as the perfect vessel for her. Abaddon warns that at that point, she will force Dean to watch as she commits atrocities with his body.
In the diner, Sam fights Jason and the second demon, but is no match for them and they are eventually joined by the third demon soldier. Sam eventually loses the fight and is knocked out, but Gadreel takes control at that point. Ezekiel displays his wings to the demons and then stuns them with a blast of white light. Once the demons are down, Gadreel kills them with the demon-killing knife so that Sam won't be suspicious when he wakes up.
As Abaddon continues to threaten Dean, she sees the blast of white light emitted by Gadreel. Realizing that the Winchesters brought an angel for backup, Abaddon throws Dean aside and teleports away.
After learning from Gadreel about what happened, Dean packs up until Sam regains consciousness. Dean claims that Sam got knocked out and Dean came to his rescue and killed the three demons by himself which he was able to do as he took them by surprise. Shortly afterwards, Tracy returns in the Impala and the three leave town.
Although Abaddon failed to get at Crowley through attacking the Winchesters, she doesn't give up her efforts to take over Hell, using Crowley's absence to start by revoking deals and collecting on the souls early. After Crowley helps free Sam from Gadreel's control, Dean releases him and he starts a war with Abaddon for rule of Hell that eventually ends with Dean killing Abaddon in battle.
- During the battle, Dean and Abaddon face off briefly one-on-one. Dean loses the fight but during a later battle, he wins a one-on-one face off with Abaddon and kills her with the First Blade.
- Sam expresses surprise that Dean was supposedly able to kill three demons alone. In First Born, Dean actually does manage to kill three demons single-handedly, impressing Cain himself with his fighting skills.