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The story is seen from various viewpoints which are tied together through the cinematic narratives presented in between each mission. They focus on the war from several perspectives:
- Lt. Colonel Voychek - an officer in Estovakian Air Force; former ace pilot now assigned to the occupation in Gracemeria as an intelligence officer
- Lt. Commander Ilya Pasternak - newly assigned lead ace tasked with destroying Emmeria's Garuda Team; placed in charge of the Strigon Squadron
- Melissa Herman - a civilian and the mother of a daughter she believes had died in the initial attack on Gracemeria, now struggling to survive the war
- Sgt. Louis McKnight - a tank officer in the Emmerian military; he leads his tank crew in following up a lead on easy money behind enemy territory, similar to the story behind the film, Kelly's Heroes
It begins in the Emmerian capital of Gracemeria, with the story of Melissa Herman as she watches her daughter getting on to a school bus for a field trip. As she watches, an enemy plane suddenly swoops in and fires on the King's Bridge, the one Matilda's school bus will be crossing, cutting it in half. Emmerian pilots are scrambled to meet what has turned out to be an all out surprise attack by the Estovakian Air Force and this is where the player is introduced into the game.
The Emmerian Air Force and Navy manage to beat back the first wave only to suffer heavy casualties from Nimbus cruise missiles launched from the P-1112 Aigaion. Ace pilots from the Estovakian Air Force's "Strigon Squadron" arrive on the heels of the attack to establish air supremacy over Gracemeria. An evacuation is ordered by Air Defense Command and all pilots are informed that the Army is planning a mass rendezvous on Khesed Island, still under the control of Emmeria.
During the next few missions, Garuda Team are tasked to assist ground forces cut off from the bulk of the Emmerian Army and eventually aid in conducting a landing at Rargom Beach in Anea, before rescuing various units trapped at Silvat Town. An eventual confrontation with the P-1112 Aigaion leads to its destruction alongside several members of the Strigon Squadron assigned to protect it, removing the threat of its Nimbus anti-air missile system in future operations. During a later mission, Air Defense Command orders all forces to suddenly pull out just as they are on the verge of success. Shamrock ignores the order and engages members of the Strigon Squadron that are in the area, forcing Talisman to assist. They are both severely reprimanded for disobeying orders. It is revealed that Estovokia is planning to detonate a chemical weapon inside Gracemeria as a last resort option should Emmeria succeed in breaking through. After a short restriction from flying, Garuda Team is tasked with the destruction of the WMD catalyst stationed at Fort Norton. After its destruction, the Emmerian military is now free to begin the Liberation of Gracemeria.
After an intense ground, naval and air battle, the Emmerians manage to liberate Gracemeria. Ilya Pasternak, the new leader of the Strigon Squadron, faces off against the Garuda Team in the skies over the city and dies fighting. Garuda and other pilots are then assigned to a night-time air patrol over the capital city in celebration. During the patrol, Shamrock reveals that his family were killed in the war and that he could not call himself an Ace since he was unable defend them. Subsequently, a surprise wave of cruise missiles are launched at Gracemeria from a previously unknown Estovakian weapon, the Chandelier, accompanied by stealth fighters which engage the pilots. Garuda Team proceeds to shoot down the missiles before any serious damage is done.
The final mission takes place deep within Estovakian territory, the only time Emmeria enters Estovakian territory throughout the game. They manage to slip past the Chandelier's defenses and damage the railgun's cooling systems but fail to destroy the weapon. Shamrock then goes on a suicide mission to locate the final weakness of the weapon by performing a recon of the loading trench below the gun to confirm the position of a backup cooling unit. With his plane heavily damaged by anti-aircraft fire, he crashes his plane into the ground. Talisman follows through with the destruction of the cooling unit, before flying into the barrel of the cannon to blast the core, destroying the Chandelier. Shamrock is later seen confined to a wheelchair having survived the crash. Lt. Colonel Voychek narrates the ending, stating that Estovakia's war was born out of desperation and convinced that it was still the right thing to do under the circumstances, but also hoping for a peaceful future between both nations.
Like previous Ace Combat games, Ace Combat 6 features an enemy ace squadron that appears as an antagonist throughout the game. Estovakia's Strigon Squadron fulfills this role, fighting the player in over a third of the game's missions. Individual aces also appear in each mission; shooting them down unlocks their aircraft's special paint scheme.
ESM support can be employed by both allied and enemy forces. ESM greatly enhances the tracking ability of guided weapons, even ordinary missiles. It also reduces the tracking ability of enemy weapons. ESM is different from jamming since it doesn't entirely prevent affected units from spotting their targets through radar and their lock-on capability is not as severely hindered.
Multiple ESM fields can overlap each other for stronger effects. Having an allied ESM field over an enemy ESM signal doesn't negate each other but the effects are still experienced by units from both sides within the field's effective range.
Frontline resupply is another feature in the game where players can land in friendly airbases to resupply, in the middle of the battle.
While the Su-33 Flanker appears primarily as an enemy plane, used by the Estovakians' elite Strigon Team, it can also be purchased and flown by the player and his wingman.
The Su-47 Berkut and F-22A Raptor are the final real-world aircraft unlocked, and are two of the game's three best-performing aircraft. The third is the last unlockable jet in the game, the fictional CFA-44 Nosferatu, which is the game's official superfighter.