Poof comes into existence when Cosmo and Wanda decide to have a child of their own, and Timmy wishes it so. However, because the fairy baby's magic is developing and uncontrollable, villains called the anti-fairies (polar opposite of fairies) and pixies (business fairies) seek to steal the fairy baby so they can take over the fairies' home, Fairy World and the Universe.

Timmy, who is tired of being the "guinea pig" of the Fairies, Pixies, and Anti-Fairies, wishes for a competition to see which one of them is the best magical creature. Jorgen does not let any fairy compete, however, because he is the strongest. When he wins the first five medals, Anti-Cosmo and HP knock out Jorgen. Timmy becomes the fairies' trainer and makes a bet: if Anti-Cosmo wins, Timmy will be his godchild; if HP wins, Timmy will work for him forever; and if Timmy wins, he will force HP and Anti-Cosmo to do something very bad. The fairies win, and Timmy says "nothing" for what Anti-Cosmo and HP do. Timmy says he learned that cheaters only cheat against themselves. It turns out to be a dream for Scott Hamilton (who was previously co-hosting the games with Timmy), because when he says what Timmy said, Juandissimo and Cupid give him a cheetah (a running gag involves that when anyone says cheater on the field or somewhere else other than the stands, Cupid gives them a cheetah).

Timmy tries to find a safer job for Catman (a.k.a. Adam West) after constant injury, but each job leads to someone or something getting attacked.

Timmy looks forward to his birthday until Jorgen reminds him that each birthday draws him a year closer to losing his fairies; however, Timmy is not worried because his parents always forget his birthday, but he then panics when they seem to remember it this year.

After a strange morning where his fairies disappear and no one at home or school remembers him, Timmy is thrust into an age-old prophecy that contains an enemy called The Darkness, and the Chosen One, who happens to be Timmy himself. Timmy finds himself traveling to Las Vegas to secure an ancient 'White Wand' after solving an ancient riddle, but he must keep ahead of The Darkness' agents, The Eliminators, as well as MERF, an extra-terrestrial secret organization that has labeled Timmy for arrest. Meanwhile, Mom, Dad, and Crocker drive to Middle Aged Rock Festival (M.A.R.F.) to prove they are still young, but constantly stop for bathroom breaks.

After beating The Darkness in "The Big Beginning", Timmy has relaxed into celebrity status on Fairy World. Turbo Thunder has become a laughing stock and a beggar after proclaiming the Darkness will come back, and Jorgen finally banishes him. Wanda, concerned that Timmy needs to get back to Dimmsdale and be normal again, poofs him back home. Meanwhile, on Yugopotamia, the Eliminators invade and steal the Yugopotamians' Fake-i-fiers, which allow them to change shape. Mark Chang, the Prince, is the only one who escapes, and heads to Earth to seek help from Timmy. Timmy, back on Earth, learns of The Darkness' return after an Eliminator disguised as Mark tries to capture him. Timmy and the gang return to the Cave of Destiny on Fairy World, where Timmy learns of a second wand located on a Blue Moon, but before he can try to make sense of anything, the Eliminators capture Jorgen, Cosmo, Wanda, and Poof, while Timmy and Mark escape through a portal back to Timmy's room. The Eliminators also round up Chester, A.J., Trixie, Mom, and Dad, and disguise themselves to capture Timmy. Timmy's normal friends and family meet his fairies and devise an escape plan using Poof's movie ninja skills. Back on Earth, Timmy and Mark recruit his enemies Crocker, Vicky, and Dark Laser to assist him. The five go to a space cantina on their way to the Blue Moon in the Vegan system. While Crocker, Vicky, and Dark Laser are caught by Eliminators disguised as patrons, Timmy and Mark are saved by Turbo Thunder, who merely uses them for information and discards them. Timmy's friends and fairies rescue his enemies and poof to the Blue Moon of Vegan just in time to save him from the Eliminators. Timmy locates the Wind Wand, but it fails to do anything. The Darkness arrives and Timmy's army is almost sucked in, forming a long chain with Jorgen at the end to save themselves. Timmy realizes The Darkness only wants him, and he decides to sacrifice himself to save the others, leaving them to mourn.

Confident and secure, Timmy feels great after defeating The Darkness as his world turns into a paradise for him; however, he soon discovers that it is all an illusion and that he did not win, but is now living inside The Darkness. Now, his family, his friends, and even his enemies on the outside must rescue him and help him find the third and final wand in order to defeat The Darkness once and for all.