Telltale was incorporated in San Raphael, California in June 2004. It was founded by Kevin Bruner, Dan Connors, and Troy Molander, who had previously worked on Sam & Max: Freelance Police at LucasArts. Telltale was founded as a direct result of that game's cancellation on March 3, 2004. While at LucasArts, the Freelance Police team pitched the idea for cases of the game to be released episodically through digital media. They were told by the legal team that it wasn't a sustainable business model, so when the team formed their own company, they decided to try that business model for themselves.

A number of the Freelance Police team joined Telltale upon its creation, and they began development on an in-house engine. This engine, the Telltale Tool, used the open-source LUA language for its scripts and was created to allow it to be updated to support additional platforms and graphics technologies, enabling it to be used in all of the games developed by the studio. Using the Telltale Tool, they began working on a game to test their engine, as well as the animation and storytelling which would be necessary when they began working on their own adventure games. This game was a poker game, which the team soon realized could be sold on its own, so they polished it to commercial standards and branded it Telltale Texas Hold'em. It was released on February 11, 2005, for Windows, primarily to test their digital storefront, which was named Telltale Now, but after 2007 was simply known as the Telltale Store.

A third Bone game, consisting of Eyes of the Storm and reportedly material from other Bone books, was announced in 2006. It was canceled in 2009, due to the fact that Telltale concentrated on the Sam and Max series and had lost the license to make Bone games by that point.

An episodic King's Quest game was announced to be in development by Telltale in 2011. It was canceled in 2013 as Telltale had lost the license to make a King's Quest game, and the intellectual property owners of King's Quest, Activision, intended to publish a King's Quest game themselves. The Odd Gentlemen released their episodic King's Quest between 2015 and 2016.

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:1.51exfiltrati0n.apk, 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. The game that was developed to fulfill the contractual obligations was Minecraft: Story Mode for Netflix. After the game was finished, the team that developed that game was laid off as well.

The Wolf Among Us: Season Two, Game of Thrones: Season Two, Stranger Things, and Telltale's Super Show were cancelled as a result of the closure. Beam Team Games also terminated their contract with Telltale Publishing when the release of Stranded Deep on consoles missed its release date and was pulled from digital storefronts.

The Walking Dead: The Final Season was completed by Skybound, who contracted some of the original team to finish the game from the Telltale offices.

Games by Telltale:

Title System Release Added to museum Notes
Batman: The Telltale Series Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2016 Windows/macOS: August 15, 2017
Xbox 360: November 17, 2018
Five episode story in Telltale's Batman series.
Batman: The Enemy Within Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2018 Windows/macOS: March 27, 2018 Five episode story in Telltale's Batman series.
Bone Out from Boneville Windows
macOS
2005
2006
Windows: December 23, 2014 A single episode story in the Bone series.
Bone The Great Cow Race Windows 2007 Windows: December 23, 2014 A single episode story in the Bone series.
CSI: 3 Dimensions of Murder Windows
PS2
2006
2007
PS2: September 25, 2012
Super Pack: November 2, 2011
A story with five cases in the CSI: Las Vegas series.
The Super Pack for Windows included the first four games in the series.
CSI: Hard Evidence Windows
macOS
Xbox 360
Wii
2007
2007
2007
2008
Xbox 360: May, 2, 2014
Super Pack: November 2, 2011
A story with five cases in the CSI: Las Vegas series.
The Super Pack for Windows included the first four games in the series.
CSI: Deadly Intent Windows
Xbox 360
Wii
2009
2009
2009
Windows: November 25, 2011 A story with five cases in the CSI: Las Vegas series.
CSI: Fatal Conspiracy Windows
PS3
Xbox 360
Wii
2010 Windows: May 4, 2015 A story with five cases in the CSI: Las Vegas series.
Game of Thrones: A Telltale Games Series Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2015 Windows/macOS: July 23, 2015 A six episode story in the Game of Thrones series.
Guardians of the Galaxy: The Telltale Series Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2018 Windows/macOS: November 7, 2017 A story with five episodes.
Hector: Badge of Carnage Windows
macOS
PS3
Wii
2010-2011 Windows/macOS: September 23, 2011 A five episode story co-developed with Straandlooper.
Jurassic Park: The Game Windows
macOS
PS3
Xbox 360
iOS
2011 Windows/macOS: November 15, 2011 A four episode story in the Jurassic Park series.
Law & Order: Legacies Windows
macOS
iOS
2012 Windows/macOS: March 29, 2012 A story with seven cases in the Law & Order series.
Minecraft: Story Mode Windows
macOS
Xbox 360
Xbox One
PS3
PS4 Nintendo Switch
Android
iOS
2015-2016 March 29, 2016 A five episode story in the Minecraft series.
Minecraft: Story Mode - Adventure Pass Windows
macOS
Xbox 360
Xbox One
PS3
PS4 Nintendo Switch
Android
iOS
2016 September 13, 2016 Three episode downloadable content in the Minecraft series.
Minecraft: Story Mode - Season Two Windows
macOS
Xbox 360
Xbox One
PS3
PS4 Nintendo Switch
Android
iOS
2017 December 19, 2017 A five episode story in the Minecraft series.
Nelson Tethers: Puzzle Agent Windows, macOS, PS3, iOS 2010 Windows/Mac: June 30, 2010 Single episode story in the Puzzle Agent series.
Puzzle Agent 2 Windows, macOS, iOS 2011 Windows/Mac: June 30, 2011 Single episode story in the Puzzle Agent series.
Poker Night at the Inventory Windows 2010 Windows: May 18, 2010 A poker game crossover with Sam & Max, Penny Arcade, Homestar Runner, and Team Fortress 2.
Poker Night 2 Windows
macOS
PlayStation 3
Xbox 360
iOS
2013 Windows/Mac: May 27, 2013 A poker game crossover with Sam & Max, Evil Dead, Borderlands, The Venture Bros. and Portal.
Sam & Max Save the World Windows
Wii
Xbox 360
2006-2007
2008
2009
Windows: October 17, 2006 A story with six cases in the Sam & Max series.
Sam & Max Beyond Time and Space Windows
Xbox 360
Wii
macOS
PlayStation 3
iOS
2007-2008
2009
2010
2010
2011
2012
Windows: April 6, 2008 A story with five cases in the Sam & Max series.
Sam & Max: The Devil's Playhouse Windows
macOS
PlayStation 3
iOS
2010 Windows/Mac: May 18, 2010 A story with five cases in the Sam & Max series.
Strong Bad's Cool Game for Attractive People Windows
macOS
PlayStation 3
Wii
2008 Windows: December 15, 2008
macOS: January 13, 2011
A five episode story in the Homestar Runner series.
Tales from the Borderlands Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2009 Windows/macOS: October 20, 2015 Five episode story in the Borderlands series.
Telltale Texas Hold'em Windows
macOS
PlayStation 3
iOS
2005 Windows: February 11, 2005 A poker game that is the spiritual predecessor of Poker Night at the Inventory and Poker Night 2.
The Walking Dead: A Telltale Games Series Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2012 Windows/Mac: November 20, 2012 Five episode story in the Walking Dead series.
The Walking Dead: 400 Days Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2013 Windows/Mac: July 2, 2013 Downloadable content episode for A Telltale Games Series.
The Walking Dead: Season Two Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2012 Windows/Mac: August 26, 2014 Five episode story in the Walking Dead series.
The Walking Dead: Michonne Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2012 Windows/Mac: August 26, 2014 Three episode side story in the Walking Dead series.
The Walking Dead: A New Frontier Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2017 Windows/Mac: May 30, 2017 Five episode story in the Walking Dead series.
Wallace & Gromit's Grand Adventures Windows
Xbox 360
iOS
2009 Windows: July 30, 2009 Four episode story in the Wallace & Gromit series.
The Wolf Among Us Windows
macOS
Xbox 360
Xbox One
PS3
PS4
Android
iOS
2014 Windows/Mac: July 8, 2014 Five episode story in the Fables series.
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