The fourth season of Teenage Mutant Ninja Turtles originally aired between September 10, 2005 and April 15, 2006, beginning with the "Cousin Sid" episode. Fourteen random episodes from this season were released on DVD on September 12, 2006.^[1] Much of this season focused on Leonardo, the group's leader, who became bitter, reserved and isolated following the final episode of the previous season in which he, his brothers and their master were almost killed. He went so far as to lash out at Splinter, causing him serious injury. This season is known among of fans as the darkest season of the series.^[2]

In the wake of their final battle with the Shredder, the Turtles retreat to the Jones family farmhouse to rest and recuperate, still heavily wounded and scarred. Leonardo in particular carries strong emotional scars from the battle, blaming himself for his family having to nearly sacrifice their lives to stop the Shredder. After the Turtles return to New York, they find that Hun has defected from the Foot Clan, instead returning to the Purple Dragons and transforming them from a street gang to a sophisticated crime organization. A successful raid on an Earth Protection Force train ends up being the final straw for the President of the United States, who threatens to cut the organization's funding for their repeated recent failures. Desperate to keep his organization afloat, Bishop engineers a staged alien invasion with man-made "aliens", which successfully convinces the President of his organization's value to protect the Earth. Unknown to Bishop, however, the residue from the destroyed alien clones leaks into New York City's sewers, and after coming into contact with local fauna, mutates them, triggering a massive mutant outbreak. During this outbreak, Baxter Stockman finally clones a new human body for himself, but it along with his sanity deteriorates, and he eventually drowns in the Hudson River while attacking April O'Neil. Nevertheless, Bishop brings him back from the dead in another cyborg body, deeming him too useful to lose.

In the meantime, Leo's emotional scars drive him to become progressively more hostile and surly to the point of wounding Splinter in an uncontrollable rage during a training session. Splinter sends Leo on a pilgrimage to the Ancient One, Hamato Yoshi's own master and father figure. The Ancient One is able to heal Leo's deep self-doubt and psychological scars, and takes the turtle under his wing. Back in New York, Karai takes up the Shredder's mantle, and rebuilds the Foot Clan to become a much more powerful organization, and with the help of the Foot Mystics, find the Turtles' lair and destroy it. Raphael, Michelangelo, Donatello, Splinter, and Klunk fake their deaths as they go into hiding. The Ancient One, having foreseen the attack, sends Leo back to New York, where he reunites his family and finds them a new home before defeating Karai, vowing that any further conflict between their clans will result in her death.

The Turtles struggle to fight Bishop's mutant outbreak, but things take a turn for the worse when Donnie is infected with the chemical agent responsible for the outbreak, mutating him once again. Leatherhead reports that Bishop's chemical agent is reacting violently with the Utrom mutagen already in his body, and will kill him in a matter of days. The group heads to Area 51 to ask for Bishop's aid in returning their brother to normal. Bishop agrees, but charges the Turtles with retrieving the Heart of Tengu, a relic possessed by Karai that an unknown entity has promised will grant him centuries of advancement in technology. The Turtles fulfill the agreement, and thanks to Leatherhead and Stockman's joint effort, cure Don and return him to normal. Meanwhile, Bishop inadvertently destroys the Heart of Tengu, having been fooled into doing so by the entity, who is revealed to be the Water Foot Mystic. The Heart of Tengu was an artifact that enabled the leaders of the Foot Clan to keep the Foot Mystics under their control. Now free, the Foot Mystics resolve to revive the "one, true Shredder".

In the season finale, the Turtles find themselves abducted by the mysterious Ninja Tribunal, along with four other warriors from across the globe. The 8 warriors are informed they are being drafted to combat a great evil that is poised to return, and they are taken to the Tribunal's monastery in Japan after passing their first test of character.

Teenage Mutant Ninja Turtles was produced by Mirage Studios, 4 Kids Entertainment, 4Kids Productions, and Dong Woo Animation and distributed by 4 Kids Entertainment and was aired on Fox's Saturday morning kids' block in the US.^[4] The producers were Gary Richardson, Frederick U. Fierst, and Joellyn Marlow for the American team. Tae Ho Han was the producer for the Korean team.^[4]