The characters encountered in Dust are rendered by way of photographs of professional actors given limited animation in sync with dialogue. A later game produced by the same company, Titanic: Adventure Out of Time, uses the same technique.
The game starts with an animation sequence showing the Stranger playing cards with The Kid—the game's antagonist. The Stranger discovers that The Kid is cheating and stabs him and runs out of the saloon. The Stranger finds himself in the town of Diamondback, New Mexico, a desert town. He is not treated with respect, and must make his way himself. There are numerous minigames in Dust, including blackjack and poker games where the player can choose to play honestly or cheat, and a shooting range helps prepare the player for a later segment of the game where quick draw skills are essential.
The game begins with a sort of short story. The Stranger, or you, is playing 5-card draw poker with a person named the Kid, the villain of the game in a Saloon. When the Stranger bets his knife, the Kid throws his cards down, and reveals that he has a four of a kind of Aces, with a king for good measure. It beats your full house. As he reaches out to get his share, a Saloon woman remarks that his arm reveals another Ace; meaning he cheated. Infuriurated that the Kid tried to cheat, you stab him in the hand with the knife. The Kid draws his gun, but you're a quick thinker and throw the table up as a barricade. The Kid fires into the air. The view changes to outside the Saloon. Two more shots are heard, than the Stranger runs out of the Saloon. We can hear a saloon patron yell the words, "Run, Stranger!"
After that, the Cyberflix logo flashes on the screen, followed by a series of screens depicting the Stranger walking through a hot, desolate desert. As this happens, the credits roll, and an elderly sounding narrator begins to speak.
The Stranger may have bested The Kid, but he had paid dearly for the privilege. He had no gun, no friends, and only a few dollars in his pocket. If he wanted to live longer than tomorrow, he'd have to find these things. Was he desperate? Let's be charitable; The Stranger, WAS, when we first met him, crow bait! Granted, Diamondback may not have looked like much either, still, we had everything he needed to survive!
The Stranger starts out at the entrance to the city, and meets the town drunkard Leroy. He gets quite a bit of information from him. After the chat, he makes fast friends with an old Chinese man named HELP. He gives the Stranger an old ring as a gift. Then, a man with a blue suit named Jackalope Jones walks up to the Stranger and drools information on the past two days on him. He also slips him an Ace, to cheat at the table. When the Stranger walks into the saloon, he immediately meets Nate Trotter. Nate tells him he should watch his back in this town.
Then after winning some money at the poker table, black jack game, or slot machine, the Stranger meets Oona Canute, owner of the Harddrive Saloon. The Stranger gives her the ring to go upstairs and talk to the girls. He talks to Ruby and makes a friendship. He also makes an acquaintance with Ruby's neighbor, the singer Sophie Delacasino. The Stranger proceeds to go either meet Bloodstone and rent a room at the Cactus Bed (A local hotel) or be granted a one night stay in the mayor's house by his wife.
After a night of rest, the Stranger gets advice from Jackalope. He tells him to replace his boots, and find a gun and some ammo. While doing these "chores", the Stranger talks with the townspeople. He gets to know the newspaper editor Chet Flippo, the apothecary man Mr. Watson, the banker, the stagecoach man Levon Deadnettle, the Livery man Ned Devries, the General store owner Mr. Bolivar, and Marie Macintosh, the daughter of the mayor who flirts with the Stranger. When these encounters are finished, the two town bullies, Cobb and Dell Belcher are going to burn down HELP's shop (because of the bill restricting Chinese immigration being passed that Monday) with HELP inside. the Stranger goes over and shoots Cobb Belcher. Dell surrenders. Mayor Macintosh appears and appoints the Stranger as Sheriff. Dell is thrown in jail and everybody hails the Stranger a hero.
The next day, the Stranger meets Sonoma, a native American of the Yunni tribe. She tells the stranger to find five sacred objects listed in the black book the Stranger was given to by Oona. Everybody is getting the jibblies from rumors that the Kid is coming to this town. Everybody is beginning to leave, including Mr. Watson. This becomes a problem when you are required to mix a medicine for Nate (who is suffering from depression). He gives the Stranger his flute (object #1). Then he steals a mask out of the mayor's house (object #2). That night, he breaks into the safe and obtains a Yunni tile from the bank (object #3), and wins a silver thunderbird in a poker game (object #4).
The next day, the Kid arrives and after insulting him a few times, the Stranger wins a duel and shoots the Kid before he can draw. The Stranger then retrieves the knife he lost at the poker game at the beginning of DUST (object #5). As night falls, the Stranger enters the mission and is instructed by Sonoma to go into the underworld.
When in the Underworld, the Stranger has to face four challenges. He has to play the flute to go through a portal, decipher a tile puzzle, find a skeleton in a mining maze, and arrange a sentence in Yunni language. After that, the Stranger finds the treasure, and Bloodstone. The Stranger destroys him by setting the tiles to say "Mesa Bird Kill Evil Man."
The next morning, the Stranger is invited to have five optional endings, though only four have an explanation behind them. He can either go into the ranching business with Nate Trotter, go into the lead business with the mayor, run away with Marie Macintosh, just walk away on his own, or give the treasure to Sonoma.
- Real-life journalist Chet Flippo appears as a character also named Chet Flippo (who, appropriately, runs the local newspaper).
- During the course of the adventure, the player has several (expensive) encounters with Buick Riviera, a con man. In the later Titanic, Riviera appears as a middle aged man playing cards aboard the ship. If you indicate that you've been to Diamondback, Riviera begins playing with a special set of Diamondback cards. The Titanic game includes several other references to Dust, but the presence of Buick is the most obvious.
- The doctor is named Hillary Rodham, the maiden name of Hillary Rodham Clinton.
- In a few of the endings, the narrarator signs out with, "I've got to see a man about a horse." This line is used again in Cyberflix's later game, Titanic.