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[src]
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 didn't even show himself when Dean's life hanged 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 lending John into a trap. John forgives Dean. But then they 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 fell 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 weird. 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, Dean chooses family over it.
- "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. (pause) 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 to Dean[src]
Though a father's love is no match for Hell, 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. 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.
Seasons 3, 4 & 5EditIn Season 3's Long-Distance Call, Dean gets a call from John about the demon who has his contract being in town. Dean once again shows willingness to follow John's orders without question.
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, the Impala. Its because of Dean's intervention that John buys the Impala. Then in Season 5's The Song Remains the Same, they meet again. 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 a bit of his fatherly side and tells everyone to shut up. Though John is quick to learn from Dean. Though Michael scrubbed John's memory clean of anything about meeting Dean.
After meeting Henry Winchester, 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, 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.