Prior to entering a dungeon, the player can use facilities in the Hamlet, the game's "hub-town" near the mansion to manage a roster of heroes and inventory.

A number of factors impact Affliction while in a dungeon, such as adventuring without food or light sources, witnessing the death or wounding of a fellow party member in battle, or from blights cast on them by enemies.

Allowing a hero to reach an extremely high stress level can cause them to have a heart attack, bringing them to the brink of death if not immediately tended to.

[3] The downloadable content (DLC) package "The Crimson Court" was released on June 19, 2017, for PC and August 22, 2017, for PlayStation 4,[4] introducing a Courtyard environment, a new playable class, a faction with new enemies, five new boss encounters, as well as new trinkets and Hamlet upgrade buildings.

As the player ventures into the manor, the dungeons below it and the surrounding lands, they find their Ancestor’s memoirs telling of the terrible deeds he had done in pursuit of knowledge and power, as well as personal desire.

Eventually, the player is able to enter the Darkest Dungeon itself, the source of the land's corruption, taking steps to reveal its ultimate form.

The party manages to defeat its physical form at great cost, but the Ancestor's spirit reveals to the player that this has only delayed its inevitable awakening and, by extension, the end of the world.

Director Chris Bourassa and lead designer Tyler Sigman had become friends while working at Backbone Entertainment, and had talked about the idea of building a game together, but their commitments to other studios left them unable to do so.

[10] In April 2013, they found they had the time to work on this project, and decided it was a "now or never" moment, forming British Columbia-based Red Hook Studios to develop the game.

This was an idea inspired by The Bard's Tale, but they were able to expand upon it to create interesting situations, such as having characters pulled out of rank by an enemy attack.

[13] The Affliction system was inspired by psychologically traumatized heroes, both through historical events as well as works of fiction such as Hudson from Aliens and the soldiers from Band of Brothers who are transformed by the horrors of combat; Sigman pointed to the seventh episode of Band of Brothers where a soldier watches his friends die from a shell explosion, stares transfixed at the event, and then becomes unable to fight any more, as the feeling they wanted to capture.

[14][15] Though they were also inspired by Lovecraftian horror, they did not want to use the concept of "insanity" that is common in that genre, and instead focused more on the nature of stress and how it affected the human psyche.

[11] A disembodied narrator, voiced by Wayne June, was also included to comment in a sardonic manner throughout the game, furthering the atmosphere they wanted.

[10] Art assets were created by Bourassa; in addition to the Lovecraftian nature, he wanted to give the game the look of woodcut and illuminated manuscripts, and took inspiration from artists such as Albrecht Dürer and eastern European painters.

[10] He further modernized the look by using ideas from comic book artists including Mike Mignola, Guy Davis, Chris Bachalo, and Viktor Kalvachev.

Following on the previous issues with Early Access updates, some of these features can be eliminated or their frequency reduced in the game's options menu.

[43][53][54][55][56] The Escapist awarded it a score of 4 out of 5, saying "Darkest Dungeon will kill your party, drive you insane, and leave you a gibbering mess at the Sanitarium.

"[57] IGN awarded it 9.1 out of 10, saying "Darkest Dungeon is a punishing and awesome game of tactics, management, and pushing your luck to the breaking point.

"[50] PC Gamer awarded it 88%, saying "A wonderfully executed, brilliantly stressful reinvention of party-based dungeon-crawling, Darkest Dungeon is great fun, even when it’s cruel.

"[58] Red Hook Studios reported that a week after the game's 2016 release, over 650,000 copies of Darkest Dungeon had been sold, including those from Kickstarter backers and Early Access purchases.

[17] In November 2016, about a month after the release of the PlayStation versions, Red Hook announced the game had sold more than one million copies across all platforms.

[59] Darkest Dungeon was nominated for two 2016 Independent Games Festival awards: the Seumas McNally Grand Prize and for Excellence in Visual Art and Audio.

[62] At the same NAVGTR Awards the following year, The Crimson Court DLC was nominated for "Game, Franchise Role Playing" and "Performance in a Drama, Supporting" for June.