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 Games:
2019
The final season had two out of four episodes funded by Telltale, and the other two were funded by Skybound.

2018
Bruce Wayne's adventures in Gotham continue in the second season of Telltale's Batman series.

2017
Telltale and Marvel have teamed up to create a game series project based on Guardians of the Galaxy.
The adventures of the new Order of the Stone, and friends, continue in more episodic adventures.
The survivors continue to struggle against zombies in Telltale's third season of their adaptation of The Walking Dead comics.

2016
Telltale and DC Comics have teamed up to create an episodic game based on Batman.
Telltale's cinematic choice and consequence-based cinematic story-based adventure set in the world of Minecraft.
DLC that tells a story over three episodes where Jesse and friends go on adventures through portals to try to return home.
A three episodes miniseries tells the story of Michonne when she was missing from the comics.

2015
A remaster of the episodic game starring the cast from the Back to the Future movies with improved textures and Tom Wilson as Biff.
Telltale adapts the hit HBO series based on a series of novels into an episodic game.
Telltale tells tales from the Borderlands in this episodic adaptation of the hit video game series by Gearbox.

2014
Telltale's adventure set in the world of The Walking Dead comics continues.
Telltale brings classic fables to the modern era in their adaptation of the popular comic book series.

2013
Telltale's third casual poker game stars Sam, Evil Dead's Ash, Venture Bros' Brock, Borderlands' Claptrap, and GLaDOS.
DLC for season one that tells five stories of five survivors that bridges the gap between season one and season two.

2012
Solve multiple cases with fan-favorite characters from the entire run of the Law & Order franchise.
Beware of the Walking Dead in Telltale's adaptation of the popular comic book and novel series.

2011
The episodic time-traveling adventures of the cast from the Back to the Future films.
The episodic adventures of a hot-headed foul-mouthed Detective Inspector named Hector.
Venture into Jurassic Park in this episodic adventure series by Telltale Games.
The mystery of Scoggins will finally be solved in the sequel to Telltale's puzzle adventure game.

2010
As a CSI in Las Vegas, solve five cases which all connect to an over-arching crime.
An FBI agent must solve puzzles to uncover the truth behind the closing of an eraser factory.
Telltale's second casual poker game starred Max, Strong Bad, Tycho from Penny Arcade, and The Heavy from TF2.
Telltale Games' episodic adventures of Sam & Max: Freelance Police continue with more crazy cases.


2009
Telltale's third CSI game has you working in Las Vegas with season nine's new CSI team.
Telltale developed this installment. Guybrush tries to defeat LeChuck and ends up cursing the entire Caribbean.
Telltale Games gives Aardman's famous wacky inventor and dog duo their own series of episodic games.

2008
Telltale Games' second season of the misadventures of everyone's favorite freelance police, Sam & Max.
Telltale and Videlectrix allow players to experience the Homestar Runner universe through the eyes of Strong Bad.


2007
Telltale Games lets you take on the role of a CSI once more as you solve five more cases in Las Vegas.
After a long hiatus, Sam & Max: Freelance Police is back, this time in an episodic series by Telltale Games.

2006
You assume the role of a rookie CSI as you solve five cases using equipment available at the Las Vegas crime lab.
Phoney tries to make money by convincing people to bet on his "mystery cow" in The Great Cow Race.

2005
Phoney Bone gets the Bone cousins tossed out of town. A swarm of locusts causes the Bones to get lost in a new land.
Telltale's first casual poker game. Boris Krinkle (as Leonard Stakechalmer) later showed up in Sam & Max seasons 1 & 2.

Canceled Games
Announced in 2006, canceled in 2009. An adaptation of the third, and possibly part or all of the fourth, Bone comic volume.
Announced in 2015 and canceled with the majority studio closure in 2018, the challenges of the Forrester clan were to continue.
Announced by Telltale in 2011, canceled in 2013. The Odd Gentlemen released their episodic King's Quest between 2015 and 2016.
Announced and canceled 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 canceled with the majority studio closure in 2018, the game was to affect the TV show. 
Announced in 2017, and canceled with the majority studio closure in 2018, Bigby Wolf's adventures in Fabletown were to continue.