Big game hunter Bill (Richard Brake), owner of Avex-Bio Tech, leads a hunting party with his partner Dr. Richards and best hunter Anna (Cassie Clare), where he takes wealthy participants to hunt down Graboids on Dark Island, a private area where he operates his company. Dr. Jasmine 'Jas' Welker (Caroline Langrishe) and colleague Jimmy (Jon Heder) work on the research site next to Dark Island where they were experiencing unnatural seismic vibrations. When Jas sees Bill leaving Dark Island, she along with Jimmy and friend Ishimon set out to investigate what Bill was up to and find a dead Graboid. They attempt to flee when they realize it has given birth to Shriekers, but the Shriekers kill Ishimon. Jas, knowing what Graboids are, instructs Jimmy to use coordinates provided by her son Travis to find Burt Gummer (Michael Gross). She visits Bill at his camp and learns Bill genetically bred the Graboids on the island and made them more powerful and intelligent for his hunt. He also cut off communications so nothing would stop him and his hunting party.
Jimmy finds Burt, who has now lived in isolation as a survivalist away from the government and content on being retired from anything related to Graboids. Jimmy informs him they need his help and Travis is unavailable due to being arrested in Mexico for smuggling Shrooms. Burt reluctantly agrees when Jimmy convinces him it’s his destiny. When he learns Jas is there, he nearly refuses to help due to their history and keeping Travis' birth a secret from him for so many years.
Having cleaned himself up, Burt gets to meet the crew, including tomboy Freddie (Jackie Cruz) who has a crush on Jimmy. Bill shows up to intimidate Burt and tell him to back off his hunt, but Burt isn’t afraid and warns Bill that the Graboids are a strong threat no matter what planning is implemented against them. Burt tries to gather weapons only to find out that they have no firearms to defend themselves, only a bunker from World War II which has machetes, two M2 flamethrowers, and dynamite that's unstable.
On Dark Island, the Shriekers Jas and Jimmy encountered have begun killing off members of his hunting party. Eventually, they find the Shriekers, but they, like their parent Graboid, are also superior to the originals and can now use their screams as sonic emitting weapons allowing them to pick off Bill's crew one by one. They are saved when Burt and the others arrive killing the Shriekers and one Graboid, leaving two remaining Graboids. Returning to Jas' research site, they are shocked to learn one of the Graboids made it to their location, showing signs it is much more powerful than they all realized. Burt warns Bill to call off the hunt and turn the communication system back on, but he refuses. Bill shoots Burt with a tranquilizer dart locking him and the others in the bunker.
Awakening in the bunker, everyone has been bound with zip ties. When Jimmy remembers that the boots he loaned to Burt had the laces replaced with 550 Paracord, Burt is able to saw the zip ties off. Meanwhile, Bill's hunt continues but goes wrong when the Graboid that made it to the site earlier has shown up and is subsequently dubbed "The Queen" due to its superiority. Anna quits when Bill's lust for the hunt proves too dangerous and insane.
Anna frees Burt and the others from the bunker, but they are attacked by a Graboid before they can leave. They use the dynamite to blow it up leaving only The Queen. Burt locates Bill to reason with him but is unable to convince him to give up his hunt. Bill meets his demise when The Queen finds them and devours Bill. Burt realizes The Queen is killing the weakest off until Burt, who Jimmy points out must be the Alpha, is left remaining. Burt gathers the remaining survivors and, inspired by the way his friends Valentine McKee and Earl Bassett successfully killed off an intelligent Graboid in his very first encounter with the creatures (Tremors), they plan to lead The Queen to an inactive volcano dubbed Devil's Punchbowl and lure The Queen over a plateau onto a bed of spiked dynamite.
Burt and Jimmy leave to kill off the remaining Shriekers, while Jas and the others set up the trap for The Queen. Burt and Jimmy make it to Dark Island and begin killing off the Shriekers with just machetes, one flamethrower, and a chainsaw.
They return to the research site, but find out The Queen is there waiting for Burt. The team heads to Devil's Punchbowl to execute the plan with Jimmy following behind with Burt. The pair are successfully leading The Queen into the trap, but Burt, at the last second, pushes Jimmy out of the way and lets himself be swallowed by The Queen to ensure her demise. The Queen dies from the dynamite and spikes, but Burt does not survive, much to the sadness of Jas and the others. In the end, they make a memorial for Burt, leaving behind their weapons with his signature hat and sunglasses.
During the credits, scenes of Burt Gummer from all the previous Tremors films are montaged.
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