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Homestuck begins when thirteen-year-old John Egbert (named via suggestion on the website's forums) receives a beta copy of an upcoming computer game, called "Sburb", in the mail. Installing and running the game on his computer triggers a meteor attack on his real-life house, which he survives only by being transported to another planet, thus immersing him completely within the world of Sburb. As John's friends Rose Lalonde, Dave Strider, and Jade Harley join the game with him, they learn that they have unwittingly triggered the end of the world, and that it is their duty to play the game and thereby see the story through to its completion.

As they begin to explore the world of Sburb, John and his friends are harassed by a group of twelve internet trolls who have played the game before. Further contact with the trolls reveals that they are not human at all, but an alien species actually called "trolls". As the trolls gradually become more important to the story, the narrative shifts to a side story exploring the nature of troll society and the specific sequence of events that led to these particular trolls entering the game themselves. The trolls' arc concludes with the revelation that winning the game causes the creation of a new universe, and that it was the trolls who originally created the humans' universe.