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With the Apocalypse looming, [[Crowley]] would later return the gun to the Winchesters, telling them they can use it to kill Lucifer. However when Dean uses it on him in Carthage, Missouri, the gun is able to cause pain and disorient Lucifer after Dean shoots him in the head, but does not kill the archangel. After Lucifer regained his composure, he knocks Dean back, sending him flying into a tree where he drops the gun, leaving it behind when [[Castiel]] teleported them away.<ref name="five10">[[5.10 Abandon All Hope...]]</ref> Crowley would go on to retrieve the Colt and after Lucifer's defeat, he turns the Colt along with the [[Lance of Michael]] over to one of the [[Princes of Hell]], [[Ramiel]] as a gift while offering him the throne. He declined and convinced Crowley to take the crown in exchange for keeping himself and his remaining siblings hidden from anyone and anything, and all the while threatening to incite his wrath on Crowley if he fails to hold up his end of the bargain. Crowley accepts and leaves the Lance and the Colt with Ramiel who locks the Colt away in a supernatural wall safe with his armory of supernatural armaments.
In 2017, the [[British Men of Letters]] task [[Mary Winchester]] with regaining it from Ramiel -- without telling her what the item is, or that Ramiel is a Prince of Hell. [[Mick Davies|Mick]] and his colleagues had been researching and studying the Colt extensively since then, however even he with all the lore on the Colt from the London Chapterhouse couldn't discover how Samuel Colt made it to kill almost anything supernatural, let alone create new bullets for it. The British Men of Letters later reveal their possession of the weapon to Sam who teaches them how to make new bullets with Bobby's recipe before using the Colt to kill the [[Alpha Vampire]].
Following a failed attempt to kill [[Dagon]], the Colt returns to the possession of the Winchesters who used it to kill the god [[Moloch]]. All the while, [[Mr. Ketch]] and his team had planted a surveillance system inside the [[Men of Letters Bunker]] to keep an eye on them and tried to retrieve the Colt in the process, but they eventually realize that Sam and Dean took it with them.
Castiel returned to the Bunker to talk to Sam and Dean about his temporary partnership with the angels, but it turns out to be a ruse to steal the Colt which was under Dean's pillow rather than in their safe for safe-keeping. After [[Joshua]] had tracked down Dagon through a celestial pulse caused by the Nephilim, Castiel and [[Kelvin]] went to her safe house along with Hozai and the Colt to kill both her and [[Kelly Kline]] with the remaining two bullets. He used one of the bullets to attempt to kill Dagon, but she teleported out of the way. Castiel went downstairs with every intent to kill kelly, but he couldn't do it. After Sam and Dean had caught up with them, they explained their plan to make the [[Nephilim]] into a human so both the baby and Kelly can live, but Kelly refused to let them do it because she wants her child to be born with their powers. After waiting in the Impala, Kelly had taken the keys and drove away with Castiel intending to go to [[Metatron's Cube|Heaven's Gate]], leaving the Colt with Sam and Dean. When they arrived, they discovered that Dagon had caught up with them after killing Hozai, Kelvin, and Joshua when he appeared. When Sam and Dean arrived and tried to stop Dagon from taking Kelly again, she attacked Dean and took the Colt from him. She used her powers to melt down the Colt, destroying it along with the remaining bullet in the chamber right before she died of spontaneous combustion due to the powers of Castiel and the Nephilim; [[Jack]].
