Aliases
Bert Aframian
Elroy McGillicutty
Edgar Cayce

Season 1

Twenty two years after Mary's death, John disappears, causing Dean to seek out Sam at Stanford University to help find him. The brothers are able to track him to Jericho, California. They then follow a set of coordinates they find amongst their father's things, thinking they might lead them to John. When the brothers return to their childhood home after Sam has precognitive dreams, they leave a message for John on his voicemail. John tracks them in Kansas, but does not reveal his presence while staying with the psychic Missouri Moseley.

John finally visits the brothers in Chicago, Illinois. Meg, a woman possessed by one of The Demon's children, reveals that the demon is after John. After defeating the daeva, the brothers split up from their father to keep him from Meg and The Demon. John meets back up with his sons when his old mentor, vampire hunter Daniel Elkins, is murdered. It turns out that the vampires that killed him also stole The Colt, a gun that could kill anything. The brothers and John succeed in getting the gun back and decide to go after the demon together.

When Meg threatens to kill their friends unless they deliver The Colt, John gives her a fake gun and is captured. The brothers end up rescuing him, but he becomes possessed by The Demon. Sam shoots him in the leg to try to get The Demon out. As the Winchesters flee the scene in Dean's 1967 Impala, a man possessed by a Demon hits them with a semi truck.

Season 2

After the crash, Sam and John awake in hospital with only minor injuries. However, Dean's life hangs on a thread.

John tries to get Sam to get some materials so that he can summon The Demon from the hospital where they have all ended up. He also seems to know what The Demon wants from Sam and other kids like him. He makes a deal with The Demon so that Dean can live. In return, he sacrifices The Colt and its last bullet, along with his soul.

After Dean wakes up, Sam angrily presses John about his whereabouts the night before. John waves it off, telling Sam that arguing is pointless. John then asks Sam to get him some coffee. After Sam leaves, John talks with Dean. John tells Dean to take care of Sam. He then whispers something in Deans ear. John then leaves Dean and returns to his hospital room, where he gives The Colt to someone. Sam walks by John's hospital room, where he finds an unconscious John on the floor. The doctors arrive to try to revive John, but are unable to save his life.

John Winchester's official time of death is 10:41AM. In the future episode, "Crossroads", a demon refers to John suffering in hell to tempt Dean into making a deal to resurrect him. In another episode, "Born Under A Bad Sign", the Demon Meg, who was possessing Sam, told Dean that she saw John in Hell and that he says "Howdy". However, this comment is most likely to have been made out of spite.

John returns in All Hell Breaks Loose, Part 2 when the gate to hell is opened. When The Demon is about to kill Dean, John grabs him and pulls him out of his human body. Both John and the Demon wrestle, but John is ultimately thrown off by the Demon and returns to his host body. This gives Dean enough time to grab the Colt to shoot The Demon in the heart to kill him. John then gives Sam and Dean a loving smile before becoming engulfed in a white light, seemingly putting his soul at rest.

Season 1
"Pilot", "Home", "Scarecrow", "Shadow", "Something Wicked", "Dead Man's Blood", "Salvation", "Devil's Trap"