Prologue
The Nightingale welcomes the audience to the realm of the birds, extolling its utopian virtues. Nevertheless, she confesses to an unfulfilled longing within her own soul.

Act I
Good Hope and Loyal Friend, disillusioned with their fellow men, have journeyed to a desolate region in search of the Hoopoe, king of the birds. They encounter the Wren, who is suspicious of humans, but they manage to persuade her to summon her master. Awakened from sleep, the Hoopoe-who had once been a man himself-confronts Good Hope and Loyal Friend, who declare their desire to live among the carefree birds. When the Hoopoe sighs that the birds have no real kingdom to call their own, Good Hope observes that the sky is their domain. The Hoopoe demurs, remarking that the air belongs to all creatures. Loyal Friend has a sudden brainstorm. He proclaims that the birds should build a great city in the clouds, fortified against men below and the gods above. Good Hope is skeptical, but the Hoopoe embraces the scheme wholeheartedly and summons the birds to his side, announcing that two men have arrived with a plan that will benefit the birds. The birds' first reaction is to denounce the men as wicked and treacherous. However, despite a warning from the Eagle, the Hoopoe prevails upon the mob to hear them out. Playing on their emotions, Loyal Friend harks back to a golden age when the birds were revered by men, and incites them to reclaim their lost glory. Galvanized, the birds commit to the scheme hatched by Loyal Friend, even if it means war. Good Hope is caught up in the excitement too, naively envisioning a better world within reach. Emboldened by his success, Loyal Friend demands that the birds honor him as their lord and master, and they willingly acquiesce. Amid much rejoicing, the birds rush off to begin their grand undertaking.

Act II
It is the following night. Good Hope is awakened by the song of the Nightingale. He feels revitalized, intoxicated by her sweet voice. Good Hope entreats the Nightingale to come closer, and asks her to teach him to see the world through her eyes. At first she tells him that he can never understand what it means to live in harmony with the universe, but his declaration of love sways her, and she imparts a kiss to his forehead, granting his desire. The air is filled with the voices of the scent of flowers, and Good Hope succumbs to their enchantment, sinking unconscious to the ground.

Daybreak illuminates the citadel in the sky built by the birds. Led by the Hoopoe and Loyal Friend, the birds vaunt their lofty achievement and their imminent dominion over all living things. A wedding procession makes it way through the crowd, led by the Wren, who proudly heralds the arrival of the first newlyweds to enter the great city. Everyone joins the nuptial celebration, which culminates in a ceremonial dance led by two Doves as the bride and groom. The mood is shattered when more birds rush in, clamoring that a mighty creature has broken through the barricades. The stranger enters, heavily cloaked, and the birds cower in fear. The Hoopoe and Loyal Friend challenge the intruder, who announces that he has come as a friend to admonish them; through the grace of Zeus, they have been given a chance to mend their ways and submit to the will of the gods. The birds react defiantly, whereupon the stranger reveals that he is the titan Prometheus, who himself had once rebelled against the gods and had been punished severely. Despite this dire warning and the misgivings voiced by Good Hope and the Hoopoe, Loyal Friend brashly exhorts the birds to wage war against the gods. Suddenly a terrible storm breaks forth, manifesting the wrath of Zeus, and a thunderbolt destroys the citadel of the birds. Chastened, the birds sing a hymn of praise and thanksgiving to Zeus. Loyal Friend emerges from hiding, clearly rattled but putting up a good front. Dismissing the whole adventure among the birds as a foolish lark, he urges Good Hope to return with him to the comforts of home in the city. Good Hope lingers for a moment, reflecting upon his brief encounter with the Nightingale, an experience which will live forever in his heart. As he turns to leave, the call of the Nightingale is heard once more; overwhelmed with emotion, Good Hope sets out on his journey home.