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Prior to becoming a supernatural hunter, John Winchester was a US Marine (Company Echo 21) and was awarded four medals for his service in Vietnam. His military experience made him well-versed with most man-made weapons. However, he had to learn how to cast spells and exorcise demons after his wife Mary was killed by a yellow-eyed demon on November 2, 1983 after she put their two sons Dean Winchester and Sam Winchester to bed for the night. John had since dedicated his life to hunting down the demon despite how powerful it was.

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He enlisted the help of Missouri Mosley, a psychic, who sent him to find Fletcher Gable. Fletcher is a squirmy man who has vast knowledge of the paranormal; he gives John the Winchester Journal and instructs him to record everything on his quest. He sends John off where he ends up meeting a man called Hunter after an encounter with a Hellhound. That encounter unfortunately saw John facing another family death, that of Mary's relative Jacob, who had tracked John and the two boys down.

John's first kill is in Issue #3 when Hunter takes him looking for a shapeshifter. Unfortunately, Dean witnesses the slaying while the creature was in the form of a man named Ichi. Issue #3 also brings the introduction of the Winchesters to the Harvelles at the Roadhouse.

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In the show, John was searching for the supernatural Colt revolver, which is the only known weapon able to kill the Yellow-Eyed Demon. John, along with his sons, later find the Colt in a vampire nest and he uses it to kill the leader of the nest for murdering John's mentor and friend, Daniel Elkins. John would later sacrifice his life and surrender the Colt to the yellow-eyed demon Azazel in exchange for Dean's life.

The Colt hasn't been mentioned to date in the comic but John comes across magical items from the very beginning of his quest. In this universe, one can be capable of casting magic without having to be a magical being.

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