Hayate becomes a cadet in Delta Flight under Mirage's wing and learns the basics of Valkyrie piloting the hard way. After weeks of slacking off training, he is issued a challenge by Mirage in a mock battle, where he must score a hit on Mirage before the time limit or he will be expelled from the unit. Meanwhile, Freyja is also struggling in her practices with Walküre, unable to find the proper motivation to sing. In order to encourage her, the Walküre members show footage of Hayate's mock battle with Mirage. Upon seeing Hayate struggling against her superior piloting, Freyja begins to sing with purpose, which seemingly also gives Hayate the motivation he needs to finally score a hit on Mirage. Mirage is shocked at how Hayate was able to beat her, but Hayate, having been impressed with Mirage's flying skills, promises to start attending her training sessions from now on.

On the planet Randall, the time comes to Freyja's first concert as a member of Walküre, as well as Hayate's first sortie as a member of Delta Flight. Everything runs well until the Aerial Knights strike again, while at the same time causing a mass Vár outbreak. Mikumo and Freyja begin singing in unison to stop the outbreak, and the other Walküre observe how Freyja's song seems to amplify Mikumo's, managing to suppress the Vár outbreak on their own. Meanwhile, the Aerial Knights reveal that while they have been distracting Walküre and Delta Flight, they had successfully seized the planet Voldor with their army and announce a declaration of war from the Kingdom of Wind to the New Unified Government.

Following the Windermere Kingdom's declaration of war on the New United Government, Delta Flight and Walküre are given new orders to defend Ragna from upcoming attacks. When rumors of Freyja being a Windermerean spy surface, she and Hayate take a joyride in his Siegfried unit to clear their heads.

The Aether is sortied to counter another Vár Syndrome infection on a New U.N. Spacy squadron, but tensions arise when Mirage is outnumbered in a dogfight and the Aerial Knights come close to killing Walküre, and Hayate is forced to stain his hands with blood for the first time in order to protect her.

Walküre and the Delta Flight perform a covert mission to planet Voldor to learn more about the enemy's plans. On the occasion, they explore ancient ruins built by the Protoculture civilization, where they discover the truth behind the proliferation of Vár Syndrome outbreaks.

Hayate, Freyja, and Mirage are confronted by the Aerial Knights while Messer and the rest of Walküre make a last-ditch effort to rescue them. During their escape, Walküre and the Delta Flight confront the Knights once more, and Hayate faces off against an infected N.U.N.S. ace pilot for the sake of returning him to his children.

Shortly after returning to Ragna, Hayate is revealed to have fold receptors in his body, which is why he resonates flawlessly with Freyja and is immune to the Vár Syndrome. Hayate and Mirage confront Messer over his Vár Syndrome infection, before accidentally discovering a song recorded by Kaname. As the duo attempt to help him, their closeness brings a lingering feeling of anxiety to Freyja, when suddenly, the Aerial Knights launch an attack on Ragna itself.

Due to his infection, Messer is relieved from the Delta Flight and reassigned to work as an instructor, but not before showing his gratitude to Kaname. Meanwhile, the Windermereans learn how to use the power of the ruins to their favor and launch an attack on the planet Al Shahal. Walküre and Delta Flight face a tough battle there against the Aerial Knights when Messer returns to assist them. In the occasion, Keith challenges him in order to settle their rivalry once and for all.

As Walküre and Delta Flight pay their respects to the fallen Messer, Arad and Kaname discover the pattern between the Protoculture ruins that could potentially bring the eight billion inhabitants of the Brísingr Cluster under control of the Vár Syndrome. Meanwhile, Grammier VI assumes direct control of the Windermere Kingdom's forces and launches a salvaged ancient ship from the Protoculture civilization for a full-scale assault on the New United Government.

Al Shahal has fallen to the Windermere Kingdom and all remaining forces still loyal to the New United Government gather on Ragna, which is their final line of defense. Knowing that the Windermereans' plan can only work with all Protoculture ruins operational, the Government makes preparations to destroy the ruins on Ragna, despite the possible consequences to the planet's environment. As the population evacuates, the members of Chaos convince the military to delay their plan to blow up the ruins as they take off with their fortress, the Macross Elysion, to commence Operation Einherjar (オペレーション・エインヘリャル Operēshon Einheryaru) confront the enemy forces.

Just as the Macross Elysion enters Al Shahal's orbit, the Sigur Berrentz folds right in front of the full N.U.N.S. defense fleet within Ragna, but not before the Macross Elysion damages its sound wave system. The Aerial Knights scramble to defend their flagship until the system is back online. Right when the Sigur Berrentz hovers near Barrett City, the N.U.N.S. detonate a reactive bomb within the Protoculture ruins. The Windermerean flagship survives the explosion, while the ruins form a larger structure that merges with the ship, effectively amplifying Heinz's song and bringing Ragna under control of the Vár Syndrome. Chaos scrambles to evacuate as many of Ragna's citizens as possible while Delta Flight engages the Aerial Knights in a dogfight and Freyja unleashes her true potential.

With the entire Brísingr Cluster under Windermerean control, the Macross Elysion and Ragna's surviving citizens become space refugees as the Island's life support systems are on the brink of failure and Chaos is low on armament and funds to stage another attack. A breach in the Island's hull causes a loss of gravity that separates Freyja from Hayate and Mirage in the underground corridors. Freyja regroups with Walküre to calm the civilians while Hayate and Mirage race against time to get the Island's power supply back online.

The Windermerean attack force return to their home planet to bury Grammier and celebrate Heinz's coronation as the new king. The kingdom broadcasts the ceremony on all galactic networks, with Roid declaring that they will expand throughout the entire galaxy and crush the New United Government as the rightful heirs to Protoculture. Heinz's singing causes all of the Protoculture ruins in the Brísingr Cluster to rise, with the potential to amplify the Vár Syndrome across the galaxy.

Aboard the Island, Makina and Chuck plan a surprise party for Freyja's 15th birthday. Hayate and Mirage go shopping for a present while Makina, Reina, and Chuck spy on them. On the night of the party, Freyja gives a speech about her childhood on Windermere and what she did to become a member of Walküre before Hayate arrives with his gift to her.

Chaos' first act to retake the Brísingr Cluster from the Windermere Kingdom is to return to planet Voldor and infiltrate the Protoculture ruins to get them to react to Walküre's songs before collecting the data. To throw the Windermerean defenses off-guard, Chaos sends a virus throughout the Galaxy Network in the guise of a live Walküre concert while making money at the same time through online app purchases. The scheme goes as planned, but Freyja begins to show her feelings toward Hayate while the rest of the group shows concern about Mikumo's change in performance. After a brief confrontation with N.U.N.S. pilot Robert Kino, Hayate confronts Arad on why he should not be involved with Windermere, only to learn of his father's past.

Delta Flight and Walküre arrive on planet Voldor, whose climate has changed since its Protoculture ruins had risen from underground. However, the Aerial Knights arrive within the planet's orbit as a security measure. Freyja is nabbed by Kassim, who apparently has a falling out with the rest of the Aerial Knights. They quickly bond over an apple barbecue due to Freyja being from a village near Kassim's apple farm. Kassim also nabs Hayate, but he lets him and Freyja go, as he is unsure of what he is fighting for. Later, Delta Flight and Walküre reach the ruins, triggering a dogfight between Delta Flight and the Aerial Knights. The singing battle between Walküre and Prince Heinz results in major fold wave disruptions all over the Brísingr Cluster.

Hayate and Mikumo are still unconscious after the events of the last battle which resulted in the destruction of the ruins in Voldor and the liberation of its population. Berger Stone approaches the members of Chaos and despite working with the Windermereans, he claims that he is an independent contractor, just like them, and discuss with them some of his theories. In the occasion, he mentions the events occurred in The Super Dimension Fortress Macross, Macross Plus, Macross 7, and Macross Frontier, claiming that all of them are somehow related to music, and proving his theory that music is a weapon, just like it is being a key element in the current conflict and mentions rumors that Mikumo is an artificial being developed by Lady M to harness this power. He also reveals that the bacteria responsible for the Vár Syndrome originated from the Vajra, finding new hosts in humanoids after they left for another dimension. After Berger leaves, Mirage tends to Hayate, who finally awakens.

Freyja is called along Hayate for an experiment to measure the effects of her singing into his body, but concerned about his wellbeing, she finds herself unable to sing. Meanwhile on Windermere, Keith is in doubt regarding Roid's true intentions and asks his squadmates, the twins Theo and Xao Jussila, for a favor. Worried that Freyja might leave Walküre for his sake, Hayate decides to resign from the Delta Flight, but Freyja insists that she is the one who must step down, until Mirage lectures both to not relinquish their dreams and careers for each other. With Mikumo still on the medical bay and off limits to visitation, Kaname, Makina, and Reina decide to infiltrate the place in order to find her, but they are caught midway and while Makina and Reina are arrested, Kaname discovers the place where Mikumo is being held.

The Kingdom of Windermere transmits Delta waves through Heinz's song to Al Shahal, sending 85% of the planet's population into a comatose state. While in prison, Kaname, Makina, and Reina recall the time they first joined Walküre before they are eventually released for their next mission. Upon being released, Mikumo reveals to them that she is an artificial lifeform, only three years old. Meanwhile, Keith discovers that Heinz is suffering from premature aging while Roid reveals that he murdered King Grammier VI.

While the Macross Elysion leads an attack to draw the Aerial Knights' attention, Walküre and the Delta Flight start their operation to infiltrate Windermere and destroy the device that controls the Protoculture ruins to put an end to the war. However, the Aerial Knights see through their diversion and launch an attack on them nonetheless. Hayate, Mirage, Arad, and the members of Walküre manage to slip past the dimensional barrier into Windermere, but Kassim follows them close and he burns out the last of his energies in a desperate effort to stop them.

Following the crash of their shuttle, Mikumo, Makina, and Reina hide in the forest to evade detection by Windermerean forces. Freyja leads Hayate and Mirage to her village while Arad and Kaname enter an abandoned N.U.N.S. garrison. Mikumo is captured by Roid while Hayate, Freyja, and Mirage are cornered by the Aerial Knights, who confront Hayate over his father's sins and Freya over her betrayal before bringing them to the site of the dimensional bomb.

Hayate, Freyja, and Mirage are put on trial in front of Heinz and sentenced to be executed. Mikumo is brought to the Sanctum by Roid, as he sees her as the reincarnation of the ancient Star Singer. Meanwhile, Berger sneaks Arad, Kaname, Makina, and Reina to Wright Immelmann's VF-22 Sturmvogel II in the castle, revealing that the craft is fully operational. As the execution is about to commence, the VF-22 suddenly bursts out of the castle as a distraction for Hayate, Freyja, and Mirage to escape and continue their mission to destroy the Protoculture ruins. Makina is shot by a sniper while protecting Freyja, but she urges her teammates to continue singing. Roid awakens Mikumo's true power, forcing Chaos to abort their mission as she sings an ancient and deadly song that triggers premature aging in Freyja.

Chaos has failed to destroy the Protoculture Center and have lost Mikumo to the Kingdom of Windermere, but they recover the flight recorder of Wright's VF-22, revealing that he was a spy but he had deviated from his mission to destroy the capital city's Protoculture ruins; instead, he tried to drop the dimensional bomb elsewhere to keep casualties to a minimum. Berger arrives and discusses about Mikumo and the effects of delta waves. Meanwhile, Roid plans to have Mikumo sing at the newly risen Star Temple on Ragna and N.U.N.S sends the 47th Special Fleet into the Brísingr Cluster, armed with dimensional weapons. The Macross Elysion heads to Ragna for a final showdown with the Kingdom of Windermere. To display the might of the kingdom, Heinz commands Mikumo to sing the Song of the Stars, infecting the N.U.N.S. fleet with the Vár Syndrome and causing them to detonate the dimensional bombs on themselves, resulting the annihilation of the whole N.U.N.S. fleet.

With the N.U.N.S. fleet wiped out by their own weapons, the final battle on Ragna is now just between Chaos and the Windermereans. Seeing the burden of shouldering the deaths of countless lives, Heinz ponders on negotiating peace talks with the N.U.N.S. while Roid prepares Mikumo on the Star Temple. Heinz orders Mikumo to sing the Song of the Stars, sending delta waves throughout the Brísingr Cluster, only to realize that Roid's objective is to bring the entire galaxy under his sole control in a Vajra-style hive mind. As both factions are mentally trapped by Mikumo's song, Heinz urges the Aerial Knights to take down Roid while Freyja tries to free her comrades from the spell. Hayate, Freyja, and Mirage's feelings for each other enable Chaos and the Aerial Knights to break free, and the combined might of Walküre releases Mikumo from Roid's control before both factions break through the Star Stage. As Hayate, Mirage, and Freyja rescue Mikumo, Keith ends the conflict by killing Roid before he himself is consumed by the destruction of the Star Stage. In the aftermath of the battle, Heinz orders the remaining Windermerean forces to retreat as the Brísingr Cluster is freed from Windermerean control.