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Due to repeated Vajra attacks, the Frontier Colonial Fleet's government approves a proposal to initiate a long-distance fold jump to escape from the Vajra assaults. As a result, all resources are being rationed. During this time, Sheryl tries to confront O'Connor about recent events but learns some very unpleasant revelations from her former manager. Distraught, Sheryl ends up walking alone in the rain searching for Alto when she collapses on the sidewalk due to her illness. Suddenly, help arrives from an unexpected source: Alto's adoptive older brother.

As the Colonial Fleet celebrates the success of its long distance fold jump, Ranka's pet Ai-kun suddenly disappears. Ranka and Brera look for Ai-kun together, ditching the victory parade where Ranka is the guest of honor. Along the way, Brera asks Ranka who does she sing for. Ranka, who's beginning to feel doubt about her singing, starts to consider her true feelings.

Meanwhile, Alto sneaks into the Satome Estate to visit Sheryl, who tells Alto that she will no longer sing. Alto leaves in frustration to go to Ranka's concert at Mihoshi Academy, where he and Michel are participating as stunt pilots. As the concert goes into full swing and Alto realizes that Ranka is singing for him, Sheryl quietly watches from a distant hill and decides she is going to walk away, but is stopped by Michel's Zentrandi sweetheart and SMS pilot Clan Clang.

In the ongoing war against the Vajra, people lose their loved ones and their hatred grows. The effects of Mishima's conspiracy grow larger and alter the lives of everyone inside Frontier. Refusing to be a singing tool for Mishima and wanting to discover the truth about her past memories of the 117 Research Fleet, Ranka tells Alto that she loved him as she leaves the colony with Brera and her Vajra pet, "Ai-Kun" on a mission to seek out the Vajra.

The Frontier populance's hatred of the Vajra is growing by leaps and bounds, and even Alto and Luca cannot control their own hate. Meanwhile, Sheryl decides to sing again with a brand new perspective, and Luca discovers that Sheryl's singing can now generate faint fold waves like Ranka's because of her V-Type virus infection. However, this is only possible because Sheryl's infection has reached a terminal stage where it can no longer be cured. Alto learns of Sheryl's illness and promised Sheryl that he will stay by her side until the very last moment.

Due to insufficient resources in the Frontier Fleet, food is being rationed. As even oxygen is being lowered inside the colony. Alto, as he had promised, is taking care of Sheryl. They shared a peaceful dinner together that Alto prepared. Later, Alto receives a detailed briefing from SMS owner Richard Bilrer and Mishima about the nature of the Vajra, the power behind Ranka's song and the threats they pose to Frontier's survival.
Meanwhile, Brera and Ranka arrive at the Vajra home system. Despite her efforts to show that she is peaceful, the Vajras led by Ai-Kun capture Ranka while she realizes that Brera is in fact her real brother. While fighting his way towards Ranka, Brera encounters O'Connor and she tells him also that Ranka is his biological sister, but then takes total control over him using an obedience override in his cybernetic implants.
The fold waves from Ranka's song are detected by both Macross Quarter and the Frontier Fleet. Having pinpointed the location of the Vajra home system thanks to Ranka's song, both the Macross Quarter and the Frontier fleet travel toward it.

The members of S.M.S Macross Quarter investigate the truth behind the destruction of the 117th Large Scale Research fleet in a Vajra attack and Ozma finds the shadow of O'Connor's ambition present in the incident where Ranka lost her family. A photo also confirms that Sheryl is Mao Nome's biological grand-daughter. Meanwhile, the NUNS military forces of Frontier prepare for a final decisive battle to protect the fleet from the Vajra. Alto visits Sheryl before the battle and promised that he will come back to her alive, but Sheryl interrupts him with a kiss. She then begs Alto to save Ranka and gives him her last fold quartz earring.

While the Frontier fleet continues its fight against the Vajra the Macross Quarter arrives and saves Battle Frontier from an enemy attack. Captain Wilder reveals evidence that proves how leaders of Macross Galaxy fleet were behind Vajra attacks on Macross Frontier fleet and that Mishima was conspiring with them. Alto manages to contact the fleet to reveal that while fighting Brera, he managed to see the true enemy inside the giant hologram of Ranka. Having escaped death by ejecting from his VF-171EX, Alto tells the Macross Quarter crew to fire at said hologram. After the Quarter shoots it, it reveals the military flagship of the Macross Galaxy fleet, Battle Galaxy, proving that it was the true faction behind the Vajra attacks. The combined Galaxy/Vajra forces start attacking again and Island One, the main residential area of the Frontier fleet receives a fierce counterattack, becoming endangered. During the battle, Alto learns of Ranka's true situation and spurs Sheryl to help him wake her from her trance. O'Connor becomes fully connected to the Vajra Queen and starts attacking the Frontier forces with it.

Frontier forces begin to falter under the sheer firepower of the Vajra and their coordination with O'Connor's control over the Queen's body and her drones. However, Ranka now freed of O'Connor's influence begins to sing and disrupts O'Connor's control of the Vajra through her songs.

Ranka is rescued by Alto from Battle Galaxy where she was being held captive. Ranka then moves the V-type infection from Sheryl's brain into her abdomen, saving her life. Ranka and Sheryl start singing together and take the Vajra out of O'Connor's control. She makes an all-out attempt to destroy Island one, but the attack is blocked by all the Vajra who have been freed from her influence, many of them sacrificing themselves in the process. Brera and Alto fight together, eventually defeating O'Connor by severing the Vajra Queen's head and Alto using Michael's sniper rifle on her. The Vajra Queen once freed from O'Connor's control begins to sing the Aimo song that Ranka claims is a Vajra love song as all Vajra depart from the regions they were attacking.

In the end the Macross Frontier fleet lands on the Vajra planet, where all the characters reunite.