Once onboard the ship, the player begins to earn the trust of the Mourningstar's different members, all of whom are subservient to Inquisitor Grendyl. From their base aboard the ship Mourningstar, the Inquisition deploys the Operative to different sectors within Tertium to research and suppress the Nurgle infestation and cult. Zola agrees to spare the player from the death penalty by conscripting them to the Inquisition. The player rescues Explicator Zola and the two successfully evacuate the ship. During transport the Tancred Bastion is suddenly swarmed and overwhelmed by followers of the Chaos god Nurgle. The player character Operative begins the story detained aboard the prison transport Tancred Bastion for a crime determined during player creation. The game's story, written by author Dan Abnett, will focus on a squad of Inquisitorial Agents investigating a potential Chaos infiltration in the Hive City of Tertium on the industrial planet of Atoma Prime. Crafting also allows the player to upgrade their weapons and increase their stats. Progression is split between random rewards, an in-game currency that will allow the purchase of weapons and a contract system to earn a weapon of your choice. Difficulty has been divided into two variables, one affecting enemy count and the other damage received from enemies. Unlike in Vermintide 2, multiple missions will take place in the same area, some of which include optional secondary objectives that allow players to obtain better loot. All classes make use of a regenerating shield. The four classes consist of a Veteran, Zealot, Ogryn, and Psyker. Rather than a set of pre-made characters, the game allows players to customize their class, appearance, and gender.

The game uses a similar formula to that used in Fatshark's Warhammer: Vermintide 2 in which four players cooperate to defeat periodic waves of AI-controlled enemies.

A release date for the Xbox Series X/S has yet to be announced. It was released for Microsoft Windows on 30 November 2022. It is a spiritual successor to Warhammer: Vermintide series. Warhammer 40,000: Darktide is a first-person action video game set in the Warhammer 40,000 universe, developed and published by Fatshark.

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