John Winchester

John was born in 1954, presumably in Normal, Illinois, as this is where we see John Winchester when he was younger at the start of As Time Goes By. At this time, it was unknown to him that his father Henry Winchester belonged to a secret society called the Men of Letters, as had his grandfather and his great-grandfather before him. Henry also states that he bought John a little music box which played As Time Goes By from the film "Casablanca". This was to help him sleep after he took John to see "Abbott and Costello Meet the Mummy" at the drive-in one night which apparently scared the "beeswax" out of him. In 1958, he went to the club, leaving John home. However, due to the attack by Abaddon, Henry was forced to flee to 2013, where he died at the hands of Abaddon. This led John to believe that his father had abandoned him.

He left to fight in Vietnam as a Marine, and held the rank of Corporal. He later returned to Lawrence, where he worked as a mechanic. On April 30, 1973, John bought a 1967 Chevrolet Impala second-hand at Rainbow Motors, after being convinced by a stranger named Dean Vanhallen to choose the vehicle. What John was unaware of, however, was that Dean was actually his future son Dean Winchester.

John had a history with Mary Campbell, although before falling in love (under the influence of a Cupid), they couldn't stand each other. John intended to propose to Mary. When Mary ran away from her family, John was killed by Azazel as he was possessing Mary's father Samuel, prompting Mary to strike a deal. Azazel would bring John back, at the cost of allowing Azazel into her home ten years later.

Five years later, in 1978, John and Mary were visited by yet another future Dean and his brother Sam. They claimed to be Mary's cousins, as she already knew that Dean was a hunter, but John did not. John was called back to work by his boss unexpectedly, but once he got there he encountered the angel Anna Milton, also from the future. Dean, Sam, and Mary stopped her from harming John, though John learned of the existence of monsters. Later John helped prepare the Campbell house for an angel attack; Sam told him of how his father raised them into the hunter's life, at which John was disgusted (though unaware that it was John himself that would do this). Much later when Anna attacked, John was tossed outside the house. John was approached by the archangel Michael who gave permission to use his body as a vessel to save Mary from Anna, but erased John and Mary's memories.

On January 24, 1979, John and Mary had their first child, Dean. On May 2, 1983 they had their second child, Sam. On November 2, 1983, Azazel stayed true to his word and visited the house, though Mary tried to intervene. Azazel killed her as a result and destroyed the house, but John, Dean, and Sam escaped with their lives. After Mary's death John went to a psychic named Missouri Moseley. He learned the truth about Mary's past. He left Lawrence with his sons, Dean and Sam. He dedicated the rest of his life to hunting down monsters, particularly Azazel. John began his hunting "career" approximately on November 2, 1983, following the death of his wife. His primary goal, as a hunter, was to kill the Yellow-Eyed Demon, Azazel, for murdering the mother of his children.

John accumulated a vast knowledge of the supernatural, keeping a journal of the creatures he hunted. He was a well-respected hunter by his peers. John worked with several other hunters, most notably: Bobby Singer, William Anthony Harvelle, Caleb, Martin Creaser, Tara, a pastor named Jim Murphy, and a psychokinetic Fred Jones. He was described as one of the best hunters, one who hardly ever ended a hunt with the monster still alive. Despite this, Sam tells Dean that his elder brother is a better hunter than John. With Tara, they hunted and exorcised a demon protégé who informed them about the existence of the Knights of Hell and the First Blade, though John never believed in the Blade's existence. Nevertheless, he and Tara kept notes of the information they gathered. They also had a brief relationship. Later, John kept a photo of Tara in his locker.

In Something Wicked, it was shown that during his hunting career, when Dean was around ten, John left him alone with Sam to hunt a Shtriga and returned only just in time to drive the Shtriga away. John was furious at Dean leaving his brother for awhile out of boredom, because it led to the situation. It took a long time for him to trust Dean again. He also never completed the hunt as he had to take Dean and Sam to Pastor Jim's and when he returned, the Shtriga was gone and did not resurface until 2006.

His life as a hunter led to strain between him and his son Sam, who wanted to quit hunting. This lead to an argument where John told Sam if he left he would have to stay away. However, John regretted saying it, as he did not want Sam to be on his own. John would surreptitiously stop by Stanford every so often just to make sure Sam was all right. John admitted it was never his intention to raise his sons the way he did.

Around August or September of 2002, after Sam had left for Stanford University, John received a call from Kate Milligan, a nurse who had treated John several years previously in Windom, Minnesota. She informed him that they had a son named Adam who was twelve at the time. According to Adam, John "dropped everything" and drove all night to Windom. After the initial meeting, John had sporadic contact with Adam. He taught him to play poker, taught him to drive in the Impala, and bought him his first beer when he was fifteen. He also took him to ball games on his birthday. John never mentioned Adam to either Sam or Dean. They learned about him around two years after John's death. Dean suspects that John saw Adam as a second chance, a child he could raise outside of hunting and do normal father-son activities with. This may have also been inspired somewhat by Sam's recent leaving.

In Pilot, Dean visits Sam at Stanford, telling him that John has gone missing. Sam reluctantly accompanies Dean to Jericho where John was on a case, but while they find his motel room, and belongings including John's journal, he is not there. While being interrogated by the police, Dean finds coordinates that John has left for him.

Dean and Sam follow the coordinates left in their father's journal in Wendigo and land in the middle of the woods where they investigate the disappearance of several campers in Black Water Ridge, Colorado. Dean points out to Sam that Dad left his journal for them, for them to pick up where he left off - saving people, hunting things, while Sam is adamant they find Dad and Jessica's killer. Dean cautions Sam to have patience, that it will take some time. Sam asks how Dean does it, how Dad did it. Dean points out the people, to help them. He later tells Sam that they will find Dad.

By the start of Dead in the Water, Sam is getting antsy to find Dad, afraid that they will stop hunting for him. Dean assures Same he wants to find Dad too - he was with Dad while Sam was away at college. But in the meantime, they need to kill evil things.

A former client calls Dean up for help in Phantom Traveler. John and Dean helped him a while back to deal with a poltergeist, otherwise he would not be alive today, and John had mentioned Sam was away at college. Dean and Sam show up, Jerry joking that missing John he gets Sam as an even trade, although Sam disagrees. The boys have their first encounter with a demon. It is a big case, and Dean wishes Dad were there to help; Sam eches the sentiment. At the end of the case, Jerry tells them their dad will be real proud of them. As they are leaving, they find out John's cell message directs clients to Dean's cell. Sam is confused, because he had been trying to dial Dad's number fifty times, and it has been out of service. However, the message on it is from John, redirecting people to call Dean if they want help - the first sign the boys have that John is still alive.

In Bloody Mary, Dean points out that in Dad's long and varied career it is alomst never been a freak medical thing - rather, it is some sign of awful supernatural death. Later, Sam asks Dean if Dad ever found evidence that Bloody Mary was the real thing, but Dean does not know.

Sam tries testing a shapeshifter in Skin by asking Dean if Dad once faced a shapeshifter in San Antonio. However, the shapeshifter has Dean's memories and responds that Dad did not face a shapeshifter in San Antonio, but a thought form - a psychic projection - from Austin. The shapeshifter later rails at Sam, saying Dean had to stay home with Dad, and Sam got to go to college. That Dean had dreams of his own, but Dad needed him, and Sam was not around. Sam left. The shapeshifter points out that he (Dean) does everything Dad asks of him, and Dad ditched him, too.

Sam is back to trying to find Dad again in Hook Man, checking the FBI's Missing Persons Databank and running his plates for traffic violations. Dean tells Sam he does not think Dad wants to be found. Sam is worried about what Dad is doing, if he is in trouble, if he needs their help. Dean promises if they get a real lead on Dad, they will chase it down. Dean brings up the case, but Sam is not so thrilled with it, so Dean points out that Dad would check it out. Later on, when the boys were hunting down a spirit, Dean hands Dam a rock salt shotgun, and Sam is impressed that Dad and Dean figured out to put a spirit deterrent - salt, in a gun.

In Bugs, Sam is reminded of Dad chewing him out, although Dad never treated Dean that way. Dean was perfect, but Dad was all over Sam's case. Dean remembers Dad raising his voice to Sam, but claims Sam was out of line. Sam scoffs, saying it was not out of line to learn soccer than bowhunting, in which Dean defends Dad, telling Sam it is an important skill. Later Sam gives some advice, and Dean calls him on that advice, telling Sam that he is saying to the boy to ditch his family. Sam realizes that the issue is really respecting the old man - that Dean thinks Sam did not respect Dad. Sam claims he respected Dad, but he just was never good enough. That Dad was disappointed in him, because he wanted to go to school and live his life. That most dads would be proud of their kid scoring a full ride, and not toss the kid out of the house. Sam confesses to Dean that he does not think Dad would want to see him when they finally find him. Dean counters that Dad was never disappointed, he was scared. That even when they were not talking, Dad would swing by Stanford to keep an eye on Sam, to keep him safe. Sam is shocked. At the end of the case, Sam tells Dean he wants to find Dad to apologize for all the things he has said to him, knowing that Dad was doing the best he could. Dean tells him, they will find Dad, Sam will apologize, and then in five minutes they will be at each other's throats again.

Distressed at returning to his home town as they follow one of Sam's visions in Home, Dean calls Dad, leaving a voice message. While investigating the haunting at their old home, Dean and Sam visit the garage John once co-owned with Mike Guenther. He tells them some of his memories of John Winchester. John was stubborn, and he hated to lose whatever game he played. He loved Mary and doted on the boys. Right after the fire John went into shock, but afterwards he told Mike that something caused the fire. He started reading the old books and went to a palm reader. The boys figure out John went to Missouri Moseley. She helps the boys, but unbeknown to them John Winchester is in town and in contact with Missouri. He tells her he can not contact them until he knows "the truth".

Sam is calling friends and other hunters in Asylum, hoping Dad had contacted one of them, but no luck. Dean has been pouring through the journal, trying to find a clue but nothing he can really make out. Dean claims Dad writes like "friggin' Yoda". Sam suggests calling the Feds and file a missing persons, but Dean reminds him they have talked about this before. Dad would be pissed. Sam does not care, Dad should have been in Kansas, and thinks he may be dead. Dean is adamant that Dad is not dead, but is possibly hiding or busy. Just then, John sends Dean a text of coordinates from "unknown sender" to send them on a job. Sam is doubtful, since Dad can barely work a toaster, but Dean points out this is good news - Dad is alive. After they investigate, Dean remembers Dad earmarked the same asylum in his journal, pulling it out for the details. Sam realizes it is a job, and Dean declares they were going, no matter how weird it seems for Sam. Going through the asylum, Sam brings up the fact that Dad has given them an order, and Dean answers yes, they have to always follow Dad's orders. When Sam is infected, he taunts Dean by saying Dean follows Dad's orders like a good little soldier, always following Dad without question, wanting Dad's approval, and they were no closer to finding Dad than they were six months ago. At the end of the case, Dean's cell rings and Sam answers - it is Dad.

Sam answers Dean's cell to hear his father's voice in Scarecrow. Sam is worried if Dad is okay, and he assures Sam that he is, but he can not tell Sam where he is at, and to trust him. John expresses sympathy at the murder of Jessica, and for the first time reveals that he knows that what killed Mary and Jess was a demon. John tells Sam that he must stop looking for him and he starts to give Sam details of a new hunt, but Sam argues that he wants to help Dad hunt the demon, against Dad's orders. Dean grabs the phone and takes the details from Dad about couples who have gone missing near Burkitsville, Indiana, before John hangs up. Dean is impressed with all the work Dad had to go through to put together this case, and calls Dad a master. Sam leaves Dean, intending to travel to Sacramento, California, where Sam traced the call, and find Dad, to help fight the demon. Dean points out that Dad does not want their help, instead asking them to work jobs and save lives, that Dad said it was not safe and for them to stay away. Sam does not understand Dean's blind faith in their dad, which Dean says is called being a good son. During the investigation of the case, the boys talk over the phone and Dean tells Sam that Sam stands up to Dad, he always has, and for Sam to call Dean when he finds Dad. However, after Dean goes missing on the case, Sam returns saying while he still wants to find Dad, he and Dean need to stick together.

When Dean looks like he is going to die in Faith, Sam calls Dad, leaving a message, to let him know that he is going to do whatever it takes to get Dean better. Sam calls every contact in Dad's journal, and one of Dad's friends called Sam back.

In Route 666, Dean explains to Sam that he and Dad were working a job in Athens, Ohio, when he met Cassie. Later on, as Dean and Cassie are "working things out", Dean confesses to her that he is still really involved with his dad's work - which in one of the main reasons they broke up to begin with.

Sam connects to another psychic in Nightmare when he realizes that both of their dads saw their moms on the ceiling, burning up. At the end of the case, Sam tells Dean that they were lucky they had Dad growing up, for things could have gone a whole different way. Dean tells Sam that he has one advantage the other kid did not have. Sam guesses the advantage is Dad, but Dad is not there for them now. Dean correct Sam - not Dad, but him.

Starting to investigate a case in The Benders, Sam points out to Dean that Dad had earmarked this area as possible hunting grounds of a phantom attacker, based on a lot of local folklore of a dark figure coming out at night grabbing people and then vanishing.

In Shadow, Dean complains that he and Dad did fine without stupid costumes. Trying to look up an ancient symbol, Sam mentions it was not in Dad's journal. Dean figures out the symbol by calling Dad's friend. When Dean and Sam encounter Meg in Chicago and realise she is linked to the demon that killed Mary and Jess, Dean calls Dad. Getting ready to fight, Dean admits he wants them all to be a family again - Dad, Sam and him. After Dean and Sam are captured, Sam realizes the whole steup was a trap for Dad. Dean laughs, claiming Dad is not in town, although Meg tells him John is in town, and that John's weakness is his boys. John later arrives and Dean embraces him warmly. Dean apologizes to Dad, that it was a trap, but John figured it was. The demon is trying to stop John, because he is going to kill it. Sam begs to help but John does not want his boys hurt and refuses. Just as he reunites for the first time in years with Sam, seemingly putting aside their argument as he is glad to see his son, they are attacked by Daevas. Sam manages to dispel Daevas and injured, they escape. Afterward, Dean supports Dad when he says it is too dangerous for them all to be together, that Dad is more vulnerable with them, and regretfully they part. John tells them that the fight is far from over and they will see each other again.

Sam declares it was a mistake to let Dad take off, because again, they do not know where he is in Hell House.

After learning that the Shtriga he once hunted has reemerged in Fitchburg, Wisconsin, in Something Wicked, John sends the coordinates to Dean as he knows that killing the Shtriga is unfinished business for Dean. Sam is surprised that something is still breathing air after Dad went after it, implying John has about a 100% kill rate. Dean remembers Dad told him consecrated wrought iron kills it, and ultimately kills the Shtriga and finishes John's old hunt. Sam presses Dean to tell about Dad's old hunt. Dad had warned Dean to keep an eye on Sammy, but Dean had left Sam and the Shtriga ended up feeding on Sam. Back then, to keep his boys safe, John took them to Pastor Jim's, but was unable to finish the hunt because the Shtriga had disappeared. John never spoke about it again to Dean, but Dean recognized that Dad looked at him different because he had been given an order and did not listen, almost killing Sammy. After hearing Dean's memories about the Shtriga, Sam admits he has given Dean a lot of crap for always following Dad's orders, but he knows now why Dean does.

In Provenance, Sam is checking John's journal concerning murders with the same M.O. in the same area of upstate New York. John had caught the pattern, and was keeping his eyes peeled for another murder to investigate. As Sam compares the provenances for the things against Dad's journal on the murders, he figures out that it is the cursed painting of the Merchant family.

Following up on the death of the hunter and old friend Daniel Elkins in Dead Man's Blood, Dean finds a message for a mail drop, just the way Dad does it. Dean and Sam are surprised when John arrives. Elkins had The Colt, a gun that can kill supernatural beings. John is after it, as it can kill the Demon that killed Mary and Jess and avenge their deaths. Together they track the vampires that killed Elkins, although John and Sam clash almost immediately and argue. During a quiet moment, Sam and John spend more time alone. John tells Sam about the college fund he had set up when Sam was born, to show that he did not want this life of a hunter for his boys. After the attack John wanted the boys kept alive and prepared, so he became their drill sergeant instead of their father. He just could not accept the fact they were different, although Sam points out with what happened with Mom and Jess, they are more in common than anyone. After capturing Kate, the leader's lifemate, John orders Dean and Sam to clean out the nest and rescue the victims and then leave while he confronts the vampires alone. They realize that afterwards John intends to go off on his own again, to fight the Demon. Even Dean argues with this, saying they are stronger as a family, but John lays down the law. Using Kate, John draws the vampires into a meeting to exchange her for the Colt, but Kate breaks free and John is knocked unconscious. However, Dean and Sam disregard Dad's orders and rescue him, though the vampire leader Luther takes Sam as a hostage to force Dean to surrender. John quickly recovers and kills Luther with the Colt, saving Sam. The surviving two vampires retreat. Afterwards, John confronts his sons for disobeying him, but agrees that they did save his life. The experience causes John to realize that they are right and it scares him: the three of them are stronger as a family. He agrees for Dean and Sam to join him in hunting the Demon that killed their loved ones.

As Pastor Jim is killed in Salvation, the Winchesters start the hunt for the demon in earnest, following signs that John has learned are associated with its appearance, to Salvation, Iowa. Sam has a vision concerning a young woman and her baby, suggesting she is a target of the demon. John is angry that the boys had not told him about Sam's visions, but Dean stands up to Dad, reminding him that he has not been in contact with them. When Meg calls she demands The Colt, killing his friend Caleb as John listens. John plans a ruse to give her a fake Colt, as he just needs to buy a few hours so Dean and Sam can take the real Colt to kill the demon. John opens up emotionally to the boys, admitting that he wants to stop losing people they love, for Sam to go to school, for Dean to have a home, for Mary to be alive... for this to be over. Both of their plans go wrong - John is captured after the gun was shown to be a fake, and the Demon eludes the boys.

Dean and Sam turn to Bobby Singer for help in Devil's Trap, when they learn Meg captured Dad. When Meg turns up, they capture her, and manage to find out John's location, exorcising the demon. In the process of rescuing Dad, Sam tests him to make sure Dad is not possessed. Dean also ends up using a bullet to kill a demon to save Sam's life. The boys take him to a remote cabin. It is while John is telling Dean he is proud of him for using a bullet that Dean gets suspicious and realizes that Dad is possessed by the Yellow-Eyed Demon. The Demon taunts Dean and Sam, and is killing Dean when John manages to wrest control for a moment. This allows Sam to get control of the Colt. Sam can not shoot to kill, and the demon escapes. As they drive to the hospital, John berates Sam for not sacrificing him to kill the Demon, having believed that Sam agreed with him that the Demon must die at any cost. However, Sam tells him that family is more important and they can still catch up to the Demon again; they still have one bullet left in the Colt to kill it with. At this moment, a demon-possessed truck driver crashes into the Impala, leaving John and his sons injured and unconscious.

In In My Time of Dying, all the Winchesters are in the hospital with various injuries, and Dean dangerously close to death. Sam discovers John is planning to keep on pursuing the Yellow-Eyed Demon, and they argue. John promises to hold off fighting the demon until Dean recovers, but he actually summons the Yellow-Eyed Demon and makes a deal - the Colt, and his life for Dean's. Dean miraculously recovers from his coma. John has a final few moments with his sons. He tries to make some peace with Sam. After Sam leaves, John pours out his heart in telling Dean he made Dean grow up too fast, that Dean took care of the family and didn't complain. John is proud of Dean, and then reveals to Dean a secret. Moments later the deal is called in and John dies.

Dean and Sam burn John's corpse, giving him a hunter's funeral in Everybody Loves a Clown. In Children Shouldn't Play with Dead Things, Sam buries John's dog tags at Mary Winchester's grave.

Dean, in talking with Gordon in Bloodlust, remembers a hunt fondly with his Dad. Burning the critter to a crisp, Dean embraces his father's Hunter lifestyle. He also thought of his Dad as indestructible, that nothing could kill him, but suddenly he is gone and he left a hole in Dean. He cannot talk with Sam about this, but must keep his game face on. Sam, however, knows Dean is not dealing with Dad's death, and calls Dean on his crap for trying to fill the hole of Dad's death with Gordon, insulting Dad. After the hunt, Dean questions how Dad raised them to hate all things supernatural. Sam reminds him that Dad did the best he could after Mom's death.

Sam talks with Jo about John in Born Under a Bad Sign, calling him obsessed with hunting, not caring who got hurt in the crossfire. After Sam ties up Jo, he demands she tell him how her dad died. Jo explains John and Bill set a trap for hellspawn, and Bill was bait. Sam laughs at the idea that John dangled Bill like meat on a hook. The thing showed up, John jumped out too soon and the thing killed Bill. Sam taunts Jo, tells her that Bill didn't die - he was begging to see Ellen and Jo one last time holding his insides in his hands; that John killed Bill, like a sick dog. Later, when Bobby hands a beer to Sam, they toast to John. The beer was laced with holy water, so the demon Meg was revealed in Sam. After this, as the demon Meg tortures Dean, she tells Dean she saw John in Hell, and that he says "Howdy".

In the last episode of the season, when Jake Talley (one of the special children) manages to open the devil's gate in Wyoming using The Colt, John escapes from Hell where he had spent around 105 years (hell time) and saves Dean from Azazel by pulling him from his vessel. John is quickly overpowered, but his actions allow Dean time to recover the Colt. When Azazel reenters his vessel, Dean shoots him in the heart, finally killing him and completing the mission John had started over 23 years earlier. John shares a tearful moment with his sons before disappearing in a flash of white light.

When Dean is poisoned by djinn in What Is and What Should Never Be, Dean lives his life as if his mom Mary never died. In this timeline, John loved playing baseball, and died in his sleep peaceably with a stroke. Dean visits John's grave while wrestling his inner conflict, before deciding on his path.

A supernatural creature called a Crocotta imitates John's voice and tries to lure Dean to his death. Greatly missing his father, Dean believes it is truly John, though Sam is more cautious. He saves Dean from death. Dean finally admits a part of him knew it was not John.

John's background is revealed to Dean. At first, he never knew about Hunters until Mary's death ten years later; he was in fact killed by Azazel who had possessed Mary's father. Mary then made a deal with Azazel to bring John back to life in exchange for Azazel being able to come into Sam's nursery in 1983.

John is seen dropping off and picking up young Dean and Sam at Truman High School.

Calling Dean and Sam, a young Adam is found to be John's youngest son. John had a romantic affair with a young nurse Kate Milligan who patched him up after a particular hunt, which resulted in a son that he would occasionally stop by to visit. Pictures of John and Adam together show father-son bonding. Adam is told of his father's death, at first as a lie, then the truth when the Winchester hunter life became known.

When the angel Anna goes back in time to kill a young John and Mary before their sons are born (as it would supposedly stop the apocalypse from ever occurring) John meets Dean and Sam, who traveled back in time to stop Anna. He becomes aware of his wife's past life as a hunter, and is shocked people could raise their children to kill supernatural beings. (The dramatic irony being that Dean and Sam know--and the audience--that John would eventually do the same.) When they are all attacked by Anna and the angel Uriel, the archangel Michael gets permission from John to inhabit his body long enough to save the others and kill Anna. John and Mary's memories of the night are erased by Michael. A Cupid is later revealed to have been behind John and Mary's union, and that it was ordered by the "higher-ups". However, the angel also added that he can only bring the two lovers together; the love they feel afterwards is completely of their own volition.

Samuel Campbell bragged that if Dean would stick around, he would show Dean tricks John never even dreamed of in Exile on Main St.

In Death's Door, Bobby remembers John yelling at him back in 1989 over the phone. Bobby took Dean out to throw a baseball, instead of practicing with a double-barrel rifle. John told Bobby he was not Dean and Sam's dad.

In Adventures in Babysitting, John had tangled with one Betala back in the day, and had written about it in his journal. Sam had gone off John's misinformation, almost getting himself killed.

Dean remembers having his Dad haul him from place to place in Plucky Pennywhistle's Magical Menagerie.

Castiel mentions how beautiful John's handwriting is in his journal in Hunteri Heroici

Dean and Sam learn about John's early life, through his father, Henry Winchester, in As Time Goes By. Sam also becomes more accepting of John's way of raising them, knowing that he did the best he could, but the brothers are left wondering how their lives would have been different if Henry had been there to raise John. Henry was also initially disgusted that John was a hunter rather than one of the Men of Letters, but came to be proud of John after seeing how he raised Dean and Sam. The boys learn that John's journal was actually Henry's journal.

John is seen in silhouette driving the Impala when he swings by to pick up a teenaged Dean from a camp, where Dean was sent as punishment to stealing food.

Dean is approached by Crowley to help locate the First Blade which Crowley could only find one demon that knew about it: one that was captured, interrogated and exorcised by John. Checking John's journal and his lock-up, Dean and Crowley learn that John worked a case with a hunter named Tara where they did interrogate and exorcise a demon who knew about the Blade, but find no further information in John's files. Finding Tara, they learn that she and John apparently had a sexual relationship as well as a professional one and that John never believed the demon about the Blade, thinking it was just lying to get out of being exorcised. However, Tara had started searching for the Blade and she is able to give Dean and Crowley their first clue on where to look. She also indicates to Dean that she believes that John would be disgusted with him for working with Crowley despite the necessity of the situation.

While working on curing Demon Dean in Soul Survivor, Sam points out to Dean that this family is all they ever had. Dean claims they have nothing. Sam asks if he'd say that to Dad, and the demon disparages John, by responding that Dad was a prize, who brainwashed them into wasting their lives, fighting his losing battle.

In The Things We Left Behind, Dean recounts a memory from his teenaged days, of John coming to the rescue from a bad situation in which he was drunk. While working a haunting in Long Island, NY, Dean and Sam convinced their father to do the sights in NYC. That night at midnight, an underage Dean leaves a zonked Sam and John to go see the club CBGB. John tracked Dean down. "Dean Winchester!" Everyone is freaking out; no one is looking John in the eye. A man with a "Kill Everything" tattoo and a safety pin through his nose looks up and says, "Sorry sir". Later, Dean whined about how much John embarrassed him, and how Dean "hated him". John replied, "Son, you don't like me, that's fine. It's not my job to be liked. It's my job to raise you right."

In Baby, when Sam falls asleep the younger version of John is driving the Impala, playing Judy Collins' "Someday Soon" on the radio. Sam wonders what is playing, and John tells him his mom used to love the song. Sam is spooked. John says it's nice to be back behind the wheel, and that Dean has been taking care of the car and Sam. Sam wonders if this is another vision, and when John expresses concern over his son Sam tells him to stop - his father is dead. John asked when death had ever stopped a Winchester, before admitting he never wanted this life for his boys. They turned out okay, but that was on them; he did his best. Sam realizes this wasn't real. John replied he couldn't fool Sam, and that this was a dream, vision, whatever you want. The message is the same - the Darkness is coming, and only you boys can stop it. That God helps those who help themselves. Sam wants answers, but wakes up. Later, Sam tells Dean about his vision, about Dad. Sam realizes it wasn't really Dad, because whoever it was was pretending to be Dad said everything Sam wanted to hear. Sam gave the messages to Dean and they talked.

Dean and Sam remember Dad taking them to the Top Notch Wrestling matches when they were younger in Beyond the Mat. Both boys have their first crush/hero in going to see the matches. Sam, however, resented the beer and entertainment being a cheap babysitter. John would always jump up and cheer when his favorite wrestler, "The Hangman", would come out.

John Winchester's early years as a hunter were murky and vaguely represented in the series. However, a lot of other hunters, including veteran ones like Bobby Singer, all refer to John as a highly skilled and capable hunter, at least during his latter years as a hunter. Even after his death, a lot of hunters talk about him; Gordon considers his sons to have "big shoes to fill" in their father's absence. Dean and Sam stated that it was very rare (only happening once for sure) that a monster survived an encounter with John. He was also noted for being able to find ways to kill things that had no apparent weaknesses: when facing a Shtriga, Sam noted that the lore stated that it couldn't be killed by the weapons of "God or man", but John had somehow figured out that it was vulnerable to consecrated iron while feeding. How he determined this is unknown as he never actually killed the creature. However, his knowledge of lore was not complete: he was unaware that his theory about there being a cure for being a werewolf was false, he did not believe in and follow up on the First Blade, he lacked knowledge of both the vampire cure and the one for djinn poison, and he was unaware Vetalas hunted in pairs. Despite this, John had a very impressive command of lore, to the point that many times Dean and Sam consult his journal as their first source of information. Several times it alone has proven to be enough for them to identify a creature and how to kill it. However, by Trial and Error, Sam considers Dean the best hunter there is, saying that he is better than Sam and even better than John at both lore and physically hunting monsters.

Even before he become a hunter, John was well versed in firearms, battle and tactics. This was because of his tenure as a marine. His knowledge on military activities allowed him to school his own sons on how to wield and even construct firearms at an early age. He was one of the few hunters who knew of the existence of The Colt, though he considered it to be a myth until after Daniel Elkins death.

Another notable trait of John's was his incredible willpower. He was temporarily able to retake control when possessed by the demon Azazel, an impressive feat; few others have been able to retake control from even weak demons, while Azazel was one of the most powerful. The only other people to display similar levels of willpower are Bobby Singer and Sam (with Sam having overpowered the second oldest Archangel). John's willpower is also shown in how he was able to escape Hell itself while the devil's gate was open. Dean noted that if anyone had the willpower to do so, John did. He was also able to briefly overpower Azazel while just a ghost, though for only a few moments. This attack saved Dean and allowed him to finally kill John's long-time enemy.

As a descendant of Cain and Abel, John is able to host the archangel Michael.