|Species|| Human (formerly)|
|Title/Alias||Johnny (by Meg)|
|Affiliation:|| Winchester Family|
United States Marine Corps (formerly)
|Family|| Cain (ancestor)|
Henry Winchester (father)
Millie Winchester (mother)
Mary Campbell (wife)
Dean Winchester (son)
Sam Winchester (son)
Adam Milligan (son)
|Portrayed by:|| Jeffrey Dean Morgan|
Matthew Cohen (young)
When John was born he originally lived in Normal, Illinois with his parents. As a small child, his father Henry had disappeared all of a sudden. It was his belief that Henry had run out on him when the truth was that his father was part of the Men of Letters and had gone to the future to where he would meet his grown up children. He and his mother moved to Lawrence, Kansas where he eventually met Mary Campbell. In the beginning, the two of them couldn't stand each other but they eventually fell in love as they got older. John went to fight in the Vietnam War and returned to Lawrence when it was over. He was planning to ask Mary to marry him but he was then killed by Azazel who was possessing Mary's father. Mary made a deal with Azazel to bring John back to life and have a life away from hunting with him in exchange for him coming back for 'something' in ten years but he assured her it wasn't her soul. John was soon brought back to life.
John was told by Mary that his father had a heart attack to explain why he found his body on the road when he awoke. After a short time, the two of them eventually got married though Mary never told him the truth of what her family did or about the deal. For ten years, he and Mary lived together. They eventually had Dean and then Sam who they named after Mary's parents. The two of them did have their share of marital problems and arguments but they seemed to get back together eventually. On the fateful night that Azazel had come to collect, Mary had walked in him trying to feed Sam his blood and he then killed her for interrupting and set the house on fire. John got Sam to Dean and told him to run out while he tried to save Mary but he was too late.
Seeking revenge after his wife was killed by the demon Azazel, John became a hunter and raised his two oldest sons to fight the supernatural. He took his boys on the road and raised them constantly on the move. He would often leave them in a motel room for days or even weeks at a time while he took hunting jobs. He soon began to train both Dean and Sam though only Dean seemed to like these times. When Sam was 18, he received a scholarship and left for Stanford against his father's wishes. They became estranged after that. It was also after this that he learned that he had another son by the name of Adam. He decided to keep his existence secret from his boys.
When he caught a sign that Azazel had resurfaced, he took off without Dean's knowledge which prompted him to go and get Sam to learn what had happened to him. When John finally united with his boys, he told them of the Colt, a gun that could kill anything. Even Azazel. They caught up to him but Azazel escaped and his demons managed to take John hostage. His sons saved him but it turned out to be a trap when Azazel possessed him. John managed to fight and get temporary control and tried to tell Sam to shoot him with the Colt to finish this but his son was unable to and Azazel managed to escape. Soon after, the three of them were in a car crash that threatened Dean's life. To save him, John went to Azazel for a deal. Azazel agreed in exchange for both the Colt and John's soul. John agreed.
When John went to save goodbye to his boys, he gave Dean a message: To save Sam but if he couldn't then he had to kill him. John then died soon after. He was sent to Hell and spent 100 years down there under the merciless torture of the demon Alistair who tried to get him to break but John never did. When the Devil's Gate opened, John managed to escape and kept Azazel at bay long enough for Dean to kill him with the Colt and finally avenge both his wife's death and his own.