Stars Jensen Ackles and Jared Padalecki as Dean and Sam Winchester. Ever since they were little, their father has been consumed with an obsession to find the evil forces that murdered his beloved wife, and recruited his two young sons to help. They have grown up as hunters of the supernatural, but conflicts between them continue to surface.
He first appears during "Abandon All Hope" sealing a deal with the executive of a failing bank to bail it out. The brothers’ break into his angel protected mansion with the help of Jo, but are captured by Crowley's henchmen and fail to trap him in a Devil's Trap. However, he uses the Colt and kills the two underlings, informing the brothers he too wants Lucifer dead and spreads information about the Colt for them to find it. He realizes that after Lucifer is done destroying humanity he would eradicate demons after disposing of humanity. He gives the Colt to the brothers, and disappears, knowing he would be hunted for betraying Lucifer.
Later appearing during The Devil You Know, he comes to the brothers as the Colt failed; having been tracking them through a magical coin, he overhears their plan to trap Lucifer with the Horsemen rings. Being on the run from demons, he offers his assistance in tracking the last two Horsemen, through their handler Brady. Sending Dean to lure Brady downstairs, they capture him. Unable to initially break Brady, Crowley goes to a known demon nest and massacres them; leaving one alive to spread the word Brady had turned against Lucifer. While successful, the demons also plant a similar tracking coin and locate their position. Sending a hellhound to retrieve Brady, Crowley disappears, leaving the brothers to deal with the hellhound, but he returns with his own (bigger) hellhound; the two beasts battle while the brothers and the two demons escape. Brady, now a fugitive, provides the position of Pestilence; Crowley leaves while Sam takes his vengeance. Crowley then appears to Bobby, offering him a deal; his soul (which he will return once Lucifer is imprisoned), for Death's location.
He returns after the brothers and Castiel secure Pestilence; he admits that he wanted Bobby's soul to prevent the brothers from killing him after they stop Lucifer but restores Bobby's legs as goodwill. He reveals the final game plan for Lucifer; the promised swine flu vaccine, shipping out nationwide, is in fact the Croatoan virus, intent on infecting the country. While Castiel, Sam and Bobby take out a premature exportation, Dean and Crowley attempt to locate Death, finding him in a pizzeria.
After the demise of Lucifer, Bobby calls upon Crowley to secure the return of his soul but Crowley typically refuses, allowing Bobby to have ten years of life before he takes his soul. Since the downfall of Lucifer, the demons now look upon Crowley as their leader, The King of Hell, though Crowley finds their pragmatism and self-servient ways frustrating. Bobby, after many days of research, calls upon Crowley again, but this time with a better plan; having summoned the ghost of Crowley's son, who, hating his father as his father hated him, quickly revealed the location of Crowley's burial grounds. With Crowley held in a Devil's Trap, Dean and Sam hold the bones hostage and Crowley is forced to relieve Bobby of his contract. At the climax of Family Matters Crowley returns with a squad of demons, including one possessing Christian Campbell, to recapture the Alpha Vampire. He reveals that he resurrected Sam and Samuel Campbell as an investment for locating Purgatory, though he left Sam's soul in the cage as a bargaining chip. He later returns to Sam and Dean in the next episode, raising awareness to them of a possible Alpha Werewolf. He is later believed to have be killed by Castiel after revealing he cannot retrieve Sam's soul from the pit.
At the end of Mommy Dearest, it is revealed that Crowley is still alive and continuing to carry out his previous torture experiments in order to find the souls of Purgatory, which contains many powerful souls. Furthermore, he is seen to be working with Castiel.
In The Man Who Would Be King, it is revealed through flashback that Crowley approached Castiel, following the Apocalypse being averted, with a proposal that they join forces to locate Purgatory, in order to plunder it for the souls there. Crowley offers that will split the souls 50/50. He seals the deal by giving Castiel 50,000 souls from Hell. In present time, Crowley is angry that Castiel did not stop the Winchester's killing Eve, who was their key to locating Purgatory. Crowley argues that Sam and Dean should be killed, but Castiel forbids it. When Sam, Dean and Bobby get a lead on a demon close to Crowley, Castiel kills him and the demons with him. Crowley sends more demons after Sam, Dean and Bobby but Castiel kills them. When Castiel's betrayal is revealed, the Winchester's trap Castiel in a ring of Holy Oil fire and demand the truth. Crowley sends a horde of demons, and the boys and Bobby are forced to flee. Crowley arrives and releases Castiel.
Crowley kidnaps Ben and Lisa in Let It Bleed, in an attempt to make Dean stand down. He and Castiel then kidnap Elanor Visyak and torture her for information on how to access purgatory and take her blood, as she is a being from purgatory and her blood is necessary for the ritual. Castiel then renegades on his deal with Crowley, refusing him the souls. The demon then forms an allegiance with Raphael, agreeing to open the gates of purgatory for the angel in exchange for his safety. When their ritual fails and the Castiel arrives, more powerful than ever after accessing the souls from purgatory, Crowley is allowed to live- as Castiel has "plans for him".
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