Twenty years after the devastating alien invasion, the United Nations has set up the Earth Space Defense (ESD), a global defense and research program that reverse-engineers alien technology and serves as Earth's early warning system against extraterrestrial threats. Civilization has been restored and relative peace among nations exists following the human race's victory over the aliens' attacks. As the twentieth anniversary of the invasion approaches, ESD Director David Levinson meets with warlord Dikembe Umbutu and Dr Catherine Marceaux in the African state Republique Nationale d'Umbutu. They travel to an intact alien city destroyer and discover that alien survivors sent a distress call to their home world before their defeat. It is revealed that former U.S. President Thomas Whitmore, Dr Brackish Okun, and Umbutu are telepathically linked to the aliens, following personal encounters, and have visions of an unidentified spherical object. An unidentified spherical ship emerges from a wormhole near Earth's Moon, and despite objections from Levinson, is destroyed on the orders of the United Nations Security Council. Defying orders, American pilots Jake Morrison and Charlie Miller then pick up Levinson, Marceaux, Umbutu, and U.S. federal controller Floyd Rosenberg on a space tug. They head for the wreckage in the Van de Graaff crater, where they recover a large container. An alien mothership suddenly appears, responding to the distress call, and proceeds to destroy much of the Earth's planetary defenses before landing over the North Atlantic Ocean, where it starts to drill down toward the Earth's molten core. Narrowly escaping death, those on board the space tug are able to avoid capture and return to Area 51. Whitmore, Levinson, and U.S. General Joshua Adams' groups interrogate one of the aliens held in captivity at Area 51's prison facility from the war. They learn that the aliens exist in a hivemind and that one of their colossal Queens is commanding the invasion. Levinson hypothesizes that if they kill the supervising Queen, her forces will cease drilling and go dormant. An ESD aerial fleet, led by Captain Dylan Hiller, stages a counterattack, but they are caught in a trap within the mothership, leaving only a few survivors, including Dylan, Jake, Charlie, and fellow ESD lieutenant and Chinese pilot Rain Lao. In Area 51, Okun opens the rescued container and releases a giant white sphere of virtual intelligence. The sphere reveals that her mission is to evacuate survivors to a planet of refuge from worlds targeted by the aliens, whom she calls Harvesters, and unite them in an attack on the Harvesters' planet. In the mothership, all surviving ESD pilots manage to escape by hijacking enemy craft; Dylan, Jake, Charlie, and Rain navigate two Harvester fighters to pursue the Queen's personal ship, which is heading to Area 51 to extract information from the sphere about the refugee planet. Knowing the Harvester Queen has become aware of the sphere's location, the ESD hide her in an isolation chamber and use a decoy in Jake's space tug to lure the Harvester Queen's ship into a trap. Whitmore volunteers to pilot the transport ship on a suicide mission, leading the Queen's ship into a trap before detonating a bomb, thus sacrificing himself but destroying the enemy ship. However, the Harvester Queen survives by using an energy shield and a fight breaks out. Initially, the ESD soldiers' weapons cannot penetrate the Queen's shield, but after the Harvester Queen lowers her shield to fire her own weapon, a good shot by Whitmore's daughter Patricia disables her shield. This allows Dylan's party, which arrives just in time, to ultimately kill her before she can take the sphere. With the Queen dead, all the remaining alien fighters are rendered inactive, while the mothership stops drilling and retreats to space. Okun reveals that the sphere has asked humanity to lead her resistance and has offered them new technology in preparation for a potential counterattack on the Harvester's home world.