In a 1920s Lovecraftian horror setting, the player amasses and expends human and nonhuman followers alongside occult texts and tools, in discovering and then pursuing any of a number of wildly differing paths to immortality, while carefully avoiding deaths arising from starvation, despair, madness, or the attention of powerful adversaries.

Success requires partial familiarization with an intricate "Secret Histories" mythology invented for this game and for connected Weather Factory projects "Book of Hours" and tabletop RPG "The Lady Afterwards."

Cards can represent human and nonhuman NPCs, attributes such as health, passion or reason, language proficiencies, occult books and scraps of lore, rituals, day jobs, influences obtained from dream, obsessions, cities, excavation sites, magical tools and ingredients, currencies, etc.

The game ultimately has many different parallel victory and failure conditions, both based on "sane" and "insane" routes that the player's character may uncover.

Moreover, as the story progresses the player will attract attention in the form of "Hunters", agents of the suppression bureau sent to find you, and "Rivals", other cult leaders looking to attain the same secrets and power as you.

"[1] Kennedy announced the project in September 2016, providing a free simplified web-driven version of how the game would play, and with plans to use Kickstarter to raise funds for an anticipated October 2017 release date.

[7] A free update released on 22 January 2019 includes an extended end-game, where the player is challenged to take their successful cult leader and elevate them into a godlike state.

[10][11] In May 2020, a DLC named "Exile" was released, which traded the base game's lore-researching and cult-building mechanics for flight across a map of 1920s Eurasia and North Africa from close pursuit by occult gangsters.

PC Gamer liked how the trial and error gameplay could lead to experimentation, "each failure comes with a bit more knowledge of how the game works and how to avoid whichever disaster befell you the last time".

Eurogamer praised the writing, saying it evoked a feeling of "a protean clutch of riddles, scholarly marginalia, back-alley rumours and pointed epithets".

[22] According to Alexis Kennedy, Cultist Simulator's sales surpassed 35,000 units within six days of release, which caused the game to break even and generate a profit in its first week.