After Sam chose to leave the family and hunting and attend Stanford, John cut off contact with him, although he regularly visited Palo Alto to check up on him.<ref>[[1.08 Bugs]]</ref> Her and Dean continued hunting together, with Dean going on hunts on his own as he got older. Around this time John and Bobby have a falling out - -- Dean comments that the last time Bobby saw John he nearly "filled him with buckshot."<ref name="one22">[[1.22 Devil's Trap]]</ref>
In 2005, John got a lead on the [[demon]] that was responsible for Mary's death, and he left Dean in order to pursue it. He tries to keep both Sam and Dean at a distance in order to protect them. He even refuses to respond when Dean calls him when he and Sam return to Lawrence in response to Sam's visions.<ref>[[1.09 Home]] and when Sam calls to tell him Dean is dying.<ref>[[1.12 Faith]]</ref></ref> When Sam and Dean encounter the demon [[Meg]] in Chicago and realize she is linked to the demon that killed Mary and Jess, Dean calls John. He later arrives and Dean embraces him and he also greets Sam warmly, expressing some regret that it has been so long. They are attacked by daevas and are nearly killed before Sam manages to dispel them with flares. Afterward, Dean supports John when he says it is too dangerous for them all to be together, and they part with John promising that the fight is just beginning and that they will be a part of it.<ref>[[1.16 Shadow]]</ref> John eventually reunited reunites with Sam and Dean in order to obtain [[the Colt]]. As they got closer to [[the Yellow-Eyed Demon]], John was kidnapped by the [[demon]] [[Meg]], and possessed by [[Azazel]]. However Sam wasn't able to kill his father with the Colt in order to kill the demon.<ref>[[1.22 Devil's Trap]]</ref>
Following a car crash caused by a [[Trucker|demon]], John offered his own life and the Colt to [[Azazel]] to save Dean. John revealed that he has known the "truth" about Sam all along. Before he died, John warned Dean that he may have to kill Sam if he couldn't save him.<ref>[[2.01 In My Time of Dying]]</ref>