This was built upon John raising Dean in the hunting lifestyle and teaching Dean the essential skills to survive. While John was about to go hunting, he always ran down with Dean the rules. His number one rule was to watch out for Sammy. There was one night though, that Dean stepped out to play video games, and came back with a Shtriga standing over Sam. John comes in only to injure the creature and yells at Dean for not protecting Sam. This sets Dean's mind set for his childhood. Unlike Sam, Dean never really disliked the way John raised him and Sam. Dean is just as good as John in hunting, and goes on hunting missions by himself. Though he does partner with John after Sam leaves for college. Then three weeks before Dean goes to get Sam, John goes missing.
|“||This is John Winchester. I can't be reached. If it's an emergency, call my son Dean. 785-555-0179. He can help.||”|
— John Winchester
in Phantom Traveler
In order to find John, Dean goes to get Sam (who he had not talked to in 2 years). Despite John's missing status, Dean still takes John's teaching with him and uses them to convince Sam to hunt while looking for John. Dean also strongly believes that John is alive and gets this confirmation when John's unavailable number is now activated with voice mail. In Home, Dean calls John for help about their old house. John does show up, but not to Dean.
Though at the end of Asylum, John finally calls Dean's cell. When Dean gets the phone from Sam, John gives Dean orders. Dean, being the loyal son, writes it down and does what John asks. Dean continues following John's orders after all this time. John on the other hand, is trying to protect his son by not being around due to what the nature is of John's hunt. John doesn't even show himself when Dean's life hang in the balance in Faith.Dean and John are reunited in Shadow when Dean thinks they found the demon. John comes to their hotel room and Dean is relieved to see John again. Dean apologizes to John for accidentally leading John into a trap. John forgives Dean. They soon get attacked by a daeva, and due to Sam's intervention they manage to escape. Now out, Dean realizes that he and Sam are John's weaknesses and says that John needs to go on his own. Dean doesn't want to hold John back nor see him defeated. So John and Dean separate.
In Something Wicked, John sends Dean on a mission. This mission handling something that had escaped John and had attacked Sammy on Dean's watch. It was a redemption mission for Dean, so he could correct his mistake all those years ago. Dean tells Sam that because of that mistake, John began to look at Dean differently, so in turn, Dean made sure never to make a mistake like that again. Dean can't handle John's disappointment.
They are reunited though in Dead Man's Blood when John comes to join Sam and Dean on a hunt. The hunt involving vampires and the Colt. Dean is though uncomfortable when John and Sam begin arguing like in the old days. Later on in the episode, John finally reveals the truth about the colt and it can kill the demon that killed Mary Winchester. They attempt to get it back, but are foiled and forced to run. After that John sends Dean to a funeral home to get Dead Man's blood. John reveals to Sam that he wants Dean to have a home. Ready to head out, John gives out orders and heads out. This is where we first see Dean disobeying his father's orders when he comes back to save John. They all have a talk, and they decide to go hunting after this demon together.
So they head out after the demon with the Colt. Then Sam gets a vision and John gets angry with Dean about not telling him. Dean responds by saying that getting John on the phone was damn near impossible. Like when Dean called about their old house, or when Dean was near death. John gets the message and tells Dean hes right, but doesn't like the new tone Dean is using. Now with Meg is back, John asks Dean to get a fake colt, so John can buy time for Sam and Dean to get the Yellow-Eyed Demon. Dean tells Sam he'd feel better if he was backing John and if John was backing them up.John is captured by Meg, and Dean wants to go after him. So they go to Bobby Singer for help. There they manage to capture Meg Masters and exercise the demon possessing her. Dean racks Meg for information despite her being on the edge of death. Dean is willing to do anything to protect his family. Dean even brings the Colt, cause Dean could use it to save their dad. They are able to rescue John and bring him to an abandoned cabin. John comes out to talk to Dean about his actions and is acting strange. Dean realizes "John" isn't John when "John" asks for the Colt. Dean knew his father would be angry that Dean used a bullet.
It turns out that it was the yellow-eyed demon possessing John. As the demon tortures Dean, Dean begs John to save him. But it doesn't work, until Dean passes out, and John regains control. John couldn't watch himself put his son in pain. Dean also begs Sam not to kill their father. Despite having the option of killing the demon once and for all, Sam decides it's not worth losing his father..
|“||You know, when you were a kid, I'd come home from a hunt, and after what I'd seen, I'd be, I'd be wrecked. And you, you'd come up to me and you, you'd put your hand on my shoulder and you'd look me in the eye and you'd... You'd say "It's okay, Dad" Dean, I'm sorry. You shouldn't have had to say that to me, I should have been saying that to you. You know, I put, I put too much on your shoulders, I made you grow up too fast. You took care of Sammy, you took care of me. You did that, and you didn't complain, not once. I just want you to know that I am so proud of you.||”|
— John Winchester's final words to Dean
in In My Time Of Dying
|“||Back at the hospital, I made a full recovery. It was miracle. Five minutes later Dad's dead and The Colt's gone. You can't tell me there's not a connection there. I don't know how the demon was involved, I don't know how it went down exactly, but Dad's dead because of me and that much I do know.[...] You and Dad ... you're the most important people in my life. And now ... I never should've came back. I was dead. And I should've stayed dead. You wanted to know how I was feeling? Well, that's it.||”|
— Dean's guilt over John's death
in Children Shouldn't Play With Dead Things
Sometime later, Dean summons a Crossroads demon while doing a case and is propositioned a deal to bring John back in exchange for Dean's soul. He is tempted, but ultimately refuses and focuses on freeing a man named Evan from his deal. The Crossroads demon leaves, but not without telling his father didn't just die in exchange for him to live, but was sent to Hell as well. Dean's guilt increases. He admits to Sam he didn't know how was going to live with that and that John should've went out fighting, not for his sake. When Sam asks if Dean was seriously considering the demon's offer to bring his father back, Dean remains silent and instead turns on the radio, implying it was true.
|“||How am I supposed to live with that? You know ... the thought of him, wherever he is. I mean ... he spent his whole life chasing that ... that yellow-eyed son of a bitch. That was supposed to be his legacy, you know? He should've gone out fighting. Not bargaining with the damn thing. Not this.||”|
— Dean to Sam when discovers the truth of John's death
in Crossroad Blues
Over time, Dean's torment over John's last order increases after discovering Sam is meant to be used as a soldier for the Yellow-eyed demon in the coming war. He privately fears Sam will join them and fears even more John's order to kill Sam if it happens, causing Dean to be torn between obeying his father and his love for Sam. Dean later calls John an ass for giving him that order and putting that on his kid, showing a part of him also resents him.
In an alternate reality created by a djinn, John never became a hunter and was instead a softball player who died peacefully from a stroke. Despite his father still being dead, Dean was happier with how went he out and saw it simply as him finding peace. Upon the discovery of everyone he ever saved dying since he never became a hunter, Dean vents his resentment and frustration to his father's headstone for life never allowing them to be happy.
|“||All of them. Everyone you saved, every one Sammy and I saved. They're all dead. [...] It's like my old life is coming after me or something. Like it doesn't want me to be happy. Course I'd know what you'd say. 'Got hunt the djinn. It put you here, it can put you back. Your happiness for all those people's lives ... no contest.' Right? But why? Why is it my job to save these people? Why do I have to be some kind of hero? What about us, huh? Mom's not allowed to live her life, Sammy's not allowed to get married. Why do we have to sacrifice everything, Dad?!||”|
— Dean talking to John's grave in an alternate reality
in What Is And What Should Never Be
Though in the end Hell is no match for a father's love, when John climbs out of Hell and saves Dean from Azazel, John's actions buy Dean the time he needs and thanks to John's assistance, Dean finally kills Azazel and avenges Mary. After Azazel is defeated, Dean approaches his dad and John gives Dean a smile and a hand on Dean's shoulder. Then John goes to heaven knowing his boys will be alright (with the exception of Dean selling his soul). Dean is amazed by the fact that John climbed out of hell, but also happy to see his dad one more time. When Sam is unsure of John escaping, Dean reassures him, saying that the door to escape was open and he knows if anyone was stubborn enough to use the opportunity, John was. Dean also completes John's mission when he kills Azazel, finally giving him his revenge.
|“||My father was an obsessed bastard! All that crap he dumped on me about protecting Sam, that was his crap! He's the one who couldn't protect his family! He's the one who let Mom die! Who wasn't there for Sam, I always was! It wasn't fair! I didn't deserve what he put on me! And I don't deserve to go to Hell!||”|
— Dean's hidden bitterness towards his father
in Dream A Little Dream Of Me
During the climax of Season 3's Dream A Little Dream Of Me, Dean acknowledges how unfair John was to him, stating that all of the things John put on him were John's issues and nothing more. It is at this point that Dean becomes his own man, not bound by his father anymore.
In Season 3's Long-Distance Call, Dean gets a call from John about the demon who has his contract being in town. Though it's later revealed it wasn't actually John and was instead a Crocotta, it shows Dean still unquestionably trusts his father and his orders. Dean later admits to Sam he just wanted to believe John could've saved him, but knows no one can get out of this but himself.
Dean goes back to the past with help of Castiel (In The Beginning) and meets his father in a diner. There John buys Dean a coffee. Dean also advises John on his car purchase, encouraging him to choose the Impala. It's because of Dean's intervention that John buys the Impala. Dean also learned that his father was once a normal person and his mother Mary Winchester was a hunter.
During On The Head Of A Pin, Dean learned Alastair tortured John in his time in Hell and that his father had the same offer of torturing souls like him. Dean felt insignificant when learning that John never broke in the full year he was there, while Dean did the opposite and broke the seal to start The Apocalypse. After being attacked by Alastair, Dean was ashamed that he couldn't live up to his father's example.
In Jump the Shark, Dean was surprised to learn that his father had another son. He didn't believe this even thinking the young man was a monster (he was partially right) until he saw a portrait of them together at a baseball game. He was so shocked beyond words that he kept repeating his discovery until coming to terms with his father's secret and his half-brother. Dean also understood that John saw Adam as a chance to raise one son normally and agreed with Sam on Adam's cursed fate.
During Lucifer Rising, Dean stood up for his father after Bobby insulted him by labeling him a coward. Dean even seemed to consider Bobby's words of being better than John and making amends with Sam until the angels abducted him to The Green Room.
Then in My Bloody Valentine, Dean learns from a Cupid that his father and mother were made to get together for him and Sam to be born to serve as Michael and Lucifer's vessels (respectively).
As of The Song Remains the Same, they meet again after Dean time travels with Sam and Castiel, although John can't remember Dean. Dean comes to John and Mary's house under the pretense that Dean is Mary's cousin. When the truth comes out about what Dean really does, John shows a bit of his fatherly side and acts the way his sons remember him. Dean is later angry when Michael possesses John to kill Anna. Dean also learned from this that Michael could possess anyone in his family. Michael later scrubs John's memory clean of anything about meeting Dean. This event also caused Dean to worry about his fate since Michael got his father to say Yes.
During Point of No Return, Dean was reunited with his half-brother Adam (who was resurrected) and listened to his rants about how John was never truly the father he wanted. Dean's facial expression made him relate to the way John raised him.
After meeting Henry Winchester in As Time Goes By, John's long-lost father, Dean is angry on John's behalf for Henry's abandonment of his son. However, he comes to forgive Henry, telling him that he understands the pain he gets from reading John's journal detailing his life as a hunter as he feels that same pain every time he reads it. Not wanting to alter things, Dean keeps Henry from going back to be with John and the skill and ingenuity Sam and Dean display cause Henry to be proud of his son despite being a hunter, stating that although he didn't know John as a man, he knows he would've been proud of him due to Sam and Dean. The experience with Henry causes Sam and Dean to see a new side to their father and wonder what life would've been like if Henry had never left John.
While looking for the First Blade to kill the Knight of Hell Abaddon in First Born, Dean works with John's old hunting partner Tara with whom he captured, interrogated and exorcised a demon that worked with Abaddon. John apparently mentioned Sam and Dean to Tara despite them never meeting her as she knew their names, but what John told her about them is unknown. Dean is also left somewhat uncomfortable to find out that John apparently had a sexual relationship with Tara during their time together. When Dean leaves with Crowley to hunt the Blade, Tara indicates that John would not be happy to see Dean working with a demon despite the necessity of the situation. She also states Dean is like his father in a way of his hunting.
Season 11 Edit
In the episode Baby, Sam wakes up from a vision of their father and urges Dean to believe it was in fact God in disguise, however, Dean dismisses this theory. He also reveals that he still dreams of their father and a fictional creation of him teaching Dean to drive at a normal age with Sam in the backseat and a driveway to pull into.
Dean is reunited with his mother Mary after the Darkness resurrects her as a 'thank you' gift. The reunion is rather turbulent as Mary had lost 33 years of her life and finds it difficult to accept that John had raised their sons the way she didn't want. Regardless, the two make an attempt to re-connect and Dean reveals to his mother that John did speak of her from time to time. Mary laments his death and describes John as a good father, something Dean doesn't exactly agree on but he doesn't deny it either.
To help Mary adapt to the new world, Dean gives Mary his father's journal.
During Lebanon, Dean tries to expel Michael from his mind while using a magic pearl but its effects cause John to appear. John is hostile until he realizes who they are and learns that he was pulled into the future. Dean happily updates his father on what's occurred before watching him reunite with Mary. John also talks with Dean and says how proud he is of the man he became and all his achievements in hunting ending that all he ever wanted was for his son was to be happy and have a normal life with family.
After the dinner, Dean shares one last embrace with John before Sam destroys the pearl and John disappears back to 2003. Dean was sadden to witness this but accepted that it was the right choice. Meanwhile, John wakes up in the Impala during 2003. He gets a call from the Dean of that year and believed the events were a dream, before telling Dean that he's coming home. Though John was sent back to the past, it is hinted that he still remembers everything and is pleased with the outcome.