Telltale was incorporated in 2004 as a result of the cancellation of Sam & Max Freelance Police at LucasArts. Much of the Freelance Police team joined Telltale from the beginning, and some of the rest of the team joined later. However, those team members have since departed Telltale. Until 2016, they released the games they developed under the Telltale Games label.

Telltale's first foray as a publisher was in 2011, with Hector: Badge of Carnage, a game which they also shared development duties with primary developer Straandlooper.  They became a full publisher in 2015, with the forming of the Telltale Publishing label.  The first game to be published under this new label was the Jackbox Party Pack, followed by Mr. Robot, 7 Days to Die, and RGX Showdown.

In 2015, Lionsgate invested in Telltale Games to enable the two companies to co-develop original and existing intellectual properties for video games and television.

In 2018, all of Telltale's investors, including Lionsgate, pulled out of investment in the company. On September 21, 2018, Telltale announced a majority studio closure, with a staff of less than 25 staying on to fulfill contractual obligations to their board and to their partners.

Stranded Deep was scheduled to be published by Telltale Publishing, however, after the majority studio closure, the scheduled release was delayed and Beam Team Games canceled their contract with Telltale. In addition, Game of Thrones: Season Two, Telltale's Super Show, The Wolf Among Us: Season Two, and Stranger Things were canceled.

The game that Telltale was contractually obligated to finish was Minecraft: Story Mode for Netflix. After that project was completed, the team that worked on that game was laid off as well. Multiple Telltale series were pulled from digital storefronts and Telltale filed for assignment in November 2018.

On November 19, 2018, Skybound Games hired some of the staff who worked on The Walking Dead: The Final Season to complete the last two episodes of that season. Those staff members worked on contract from the Telltale offices. The final two episodes of The Walking Dead: The Final Season were released in 2019.

On August 28, 2019, LCG Entertainment announced that they had purchased Telltale and the rights to some of their games.

Games by Telltale under LCG Entertainment:
Episodic Choices-and-Consequences Game. Telltale and Deck Nine make a series based on The Expanse.
Episodic Choices-and-Consequences Game. Telltale and AdHoc Studio continue Bigby Wolf's adventures in Fabletown.

Games by Telltale:

Episodic Choice-and-Consequences Game. Two episodes were funded by Telltale and the other two were funded by Skybound.

Episodic Choice-and-Consequences Game. Bruce Wayne's adventures in Gotham continue in the second season of Telltale's Batman series.

Episodic Choices-and-Consequences Game. Telltale and Marvel created a game series project based on Guardians of the Galaxy.
Episodic Choices-and-Consequences Game. The adventures of the new Order of the Stone continue in more episodic adventures.
Episodic Choices-and-Consequences Game. Survivors struggle against zombies in Telltale's third season of The Walking Dead.

Episodic Choices-and-Consequences Game. Telltale and DC Comics teamed up to create an episodic game based on Batman.
Episodic Choices-and-Consequences Game. Telltale presents a cinematic story set in the world of Minecraft.
Episodic Choices-and-Consequences Game. DLC wherein Jesse and friends go on adventures through portals to try to return home.
Episodic Choices-and-Consequence Game. This miniseries tells the story of Michonne when she was missing from the comics.

Remastered Episodic Direct-Controlled Adventure. It features improved textures and Tom Wilson as Biff.
Episodic Choices-and-Consequences Game. Telltale adapts the hit HBO series based on a series of novels into an episodic game.
Episodic Choices-and-Consequences Game. Telltale tells episodic tales of The Borderlands in an adaption of the series by Gearbox.

Episodic Choices-and Consequences Game. Telltale's story set in the world of The Walking Dead comics continues.
Episodic Choices-and-Consequences Game. Telltale brings classic fables to the modern era in their adaptation of the Fables comics.

Poker Game. Telltale's third casual poker game stars Sam, Evil Dead's Ash, Venture Bros' Brock, Borderlands' Claptrap, and Portal's GLaDOS.
Choices-and-Consequences Game. DLC tells five stories of five survivors that bridge the gap between season one and season two.

Episodic Point-and-Click Puzzle Game. Solve cases with fan-favorite characters from the entire run of the Law & Order franchise.
Episodic Choices-and-Consequences Game. Beware of the Walking Dead in Telltale's adaptation of the comic book series.

Episodic Point-and-Click Adventure. The time-traveling adventures of the cast from the Back to the Future movies.
Episodic Point-and-Click Adventure. The adventures of a hot-headed foul-mouthed Detective Inspector named Hector.
Episodic Direct-Controlled Action-Adventure. Venture into Jurassic Park in this episodic series by Telltale Games.
Point-and-Click Puzzle Game. The mystery of Scoggins is fully revealed in the sequel to Telltale's puzzle game.

Point-and-Click Puzzle Game. As a CSI in Las Vegas, solve five cases that all connect to an over-arching crime.
Point-and-Click Puzzle Game. An FBI agent must solve puzzles to uncover the truth behind the closing of an eraser factory.
Poker Game. Telltale's second casual poker game starred Max, Strong Bad, Tycho from Penny Arcade, and The Heavy from TF2.
Episodic Direct-Controlled Adventure. Telltale's episodic adventures of Sam & Max: Freelance Police continue with more crazy cases.

Point-and-Click Puzzle Game. Telltale's third CSI game has you working in Las Vegas with season nine's new CSI team.
Episodic Direct-Controlled Adventure. Guybrush tries to defeat LeChuck and ends up cursing the entire Caribbean.
Episodic Direct-Controlled Adventure. Telltale gives Aardman's famous wacky inventor and dog duo their own series of episodic games.

Episodic Point-and-Click Adventure. Telltale's second season of the misadventures of everyone's favorite freelance police, Sam & Max.
Episodic Point-and-Click Adventure. Telltale and Videlectrix showcase the Homestar Runner universe through the eyes of Strong Bad.

Point-and-Click Puzzle Game. Telltale Games lets you take on the role of a CSI once more as you solve five more cases in Las Vegas.
Episodic Point-and-Click Adventure. After a long hiatus, Sam & Max, the Freelance Police are back, in an episodic series by Telltale.

Point-and-Click Puzzle Game. A rookie CSI solves five cases using equipment available at the Las Vegas crime lab.
Point-and-Click Adventure. Phoney tries to make money by convincing people to bet on his "mystery cow" in The Great Cow Race.

Point-and-Click Adventure. Phoney Bone gets the Bone cousins tossed out of town. A locust swarm causes them to get lost in a new land.
Poker Game. Telltale's first casual poker game features Harry Weinhead, Boris Krinkle, Theodore Dudebrough, and Grandma Shakey.

Cancelled Games
Announced in 2006 and cancelled in 2009. An adaptation of the third, and possibly part or all of the fourth, Bone comic volume.
Announced in 2015 and cancelled with the majority studio closure in 2018, the challenges of the Forrester clan were to continue.
Announced by Telltale in 2011 and cancelled in 2013. The concept became reality in an episodic game by The Odd Gentlemen in 2015.
Revealed and cancelled in 2018 with the majority studio closure. Netflix is looking for another studio to develop the game.
Announced in 2015 as a game and TV series, and cancelled with the majority studio closure in 2018, the game was to affect the TV show.