Set 11 years after the first 'Starship Troopers' movies, in the past 11 years of "The Second Bug War", the Mobile Infantry fighting the giant Arachnid bugs has improved their weapons and tactics. However, as they adapt, so do the Bugs, and many new Arachnid variants have developed whom include exploding mortar bugs, and scorpion-like tank bugs that spray lethal plasma energy bursts which disentegrates people and equipment. The militarist Earth government, now called 'The United Citizen Federation of Earth' now finds itself engaged in trench warfare on the frontier planets in many parts of the Milky Way Galaxy. The Federation puts a positive spin on this in the media while using its judicial and military authority to suppress peace protesters and religious fanatics as seditionists.Colonel John Rico (Casper Van Dien) is stationed on the agrarian planet Roku San when the popular Sky Marshal Omar Anoke (Stephen Hogan) pays a visit. Off-duty, Rico's old friend General Dix Hauser (Boris Kodjoe) gets into a bar-fight with farmers protesting the war. During the fight, Rico stops Dix from shooting one of the farmers. Dix tries to have Rico arrested, but the base defenses suddenly fail. Rico knocks Dix out and leaves to help fight the Arachnid warrior bugs that attack supported by flame-throwing Tanker bugs and energy-shooting Scorpion bugs. When the outpost at Roku San falls, Rico is blamed by the Federal Media and sentenced to death by a military tribunral for insubordination and striking a superior officer.On their way back to the moon of Sanctuary #5, the Fleet's secret HQ, Captain Lola Beck (Jolene Blalock) is marooned on a classified planet known as Planet OM-1 with Sky Marshal Anoke. Back on Earth, Admiral Enolo Phid (Amanda Donohoe) suppresses this information as not to lower public moral and support for the war then it has already detorated. Dix finds out thanks to an officer who thinks this is wrong and recruits Rico to rescue the Sky Marshal and Lola, the latter being one of the few in possession of the coordinates to Sanctuary #5, which would cripple the military if the Arachnids learned of its location.Back on OM-1, a supposed earthquake takes the life of Dr. Wiggs (Danny Keough) while the Sky Marshal views a giant eye staring back at him from below. Cynical cook Jingo Ryan (Jon Falkow) is next to die after he takes shelter from Warrior bugs within a cluster of supposed rock outcroppings, which are actually Arachnid limbs which pull him below. Engineer Bull Brittles (Stelio Savante) asks the very religious flight attendant, Holly Little (Marnette Patterson), to marry him, but he dies shortly after in another bug ambush.Meanwhile on Earth, General Hauser confronts Admiral Phid about why she is abandoning the Sky Marshal, only to be arrested. Later, Phid reveals to him that Sky Marshal Anoke is responsible for the downfall of Roku San, having been in communication with the "Brain of Brains," also known as "Behemecoatyl." It turns out that the the original brain bug captured on Planet P (from the first 'Starship Troopers' movie) is still being held in Federation quarantee and has psychic powers. With the Brain Bug acting as a conduit for Behemecoatyl, Sky Marshal Anoke adopted the bug's religion, hoping he could save humanity from the bugs if he could make peace with them. It is revealed that Anoke turned off the electric barrier surrounding the base on Roku San to show his willingness to make peace between the two species.After visiting the facilty where the Brain Bug is being held, Admiral Phid and General Hauser discuss the situation where the Federation now believes the Brain Bug allowed itself to be captured in the first place on Planet P in order to pass on intelligence from inside The Federation. The Federation makes the decision to kill and dissect the captured brain but it overhears them and unleashes a telepathic scream, killing a few soldiers before Hauser kills it. It is revealed that Admiral Phid ignored the distress calls of those abandoned on OM-1 so she could become the new Sky Marshal; however, she failed to take into account that Lola, who is one of the few pilots of the Federation that knows the location of Sanctuary, was with Anoke.Back on OM-1, the stranded survivors make contact with The Brain of Brains, who communicates with them through the corpses of their fallen comrades and soon kills Anoke for his knowledge; Lola and Holly, the last two left alive, begin to pray that they will be saved.Suddenly, Rico leads the Marauders, an elite team of troopers composed of his command staff from Roku San, on a rescue mission, using the Federation's new battle-suits. They defeat the Arachnid warriors on OM-1, suffering no casualties, and rescue the two survivors. OM-1 is revealed to be the home of the Bug Hive, the Arachnid's ruling body, and Fleet destroys it from orbit with a planet-destroying "Q Bomb."Rico is subsequently awarded a promotion to the rank of General, and given permanent command of the Marauder program. Anoke is reported to have died in a terrorist attack (staged by the government earlier to explain his disappearance) and given a hero's funeral. Dix and Lola are married, Admiral Phid is appointed the new Sky Marshal with Dix as her second-in command, and Holly becomes a Federal chaplain. Dozens of peace protesters are hanged in connection to the terrorist attack and a Christian-esque religion is embraced by the Federation (seemingly for morale and propaganda purposes) as the war continues with no end in sight.