The play begins with Peisetaerus and Euelpides attempting to make their way across a hillside with their birds directing them seemingly in no apparent direction that will get them to their destination. Euelipides has a crow and Peisetaerus, a jackdaw. The two middle-aged men have decided to seek a new land to live in as they are through with Athens, it is too much law and argument for their taste. The men are seeking Tereus, a man who has been transformed into the Hoopoe in hopes he will help them find a better way of living somewhere else.
They arrive at a door where a bird which strikes fear in them answers, he is Tereus' servant. Tereus then comes out to them and they see that he hardly has any feathers upon his body, as he says is due to molting. Peisetaerus has the idea that the birds should stop flying around aimlessly in the sky and instead build a giant city in-between the men of earth and the gods of the heavens in order that the birds can catch all of the sacrifices of man and thus have the power over the gods as they will begin to starve without the sacrifices. Tereus the Hoopoe summons the birds with a song. Upon the birds arrival they appear to want to attack the men, but are talked out of it. Peisetaerus tells the birds of a plan that will allow them to be the gods to reign over man instead of Zeus and his children. The plan for the great city is set out before them and the birds agree that it is an excellent idea.
Peisetaerus and Euelpides retire into Tereus' home in order to be transformed into birds themselves. The Chorus then gives the genealogy of the gods, in which they claim that the birds are the children of Eros and the grandchildren of Night and Erebus, giving them claim to the earth over the current gods. The middle-aged travelers come out of Tereus' home transformed, as best they could be, into birds, and proclaim that the name of the new city built by the birds will be Cloudcuckooland. Peisetaerus begins to perform religious ceremonies, sacrifices in honor of the new gods, the birds who have begun to build their great city in the sky. Upon his attempt to sacrifice, Peisetaerus is interrupted by multiple visitors which he has to run off including a Poet, an Oracle-Monger, Meton, an Informer, a Decree-Seller. Peisetaerus then returns indoors to finish the religious ceremony.
Upon his return outside, Peisetaerus is greeted by an messenger who says that the bird city is already been completed. A second messenger arrives stating that one of the gods of Olympus has broken through the bird city, it is the goddess Iris who is cornered by the birds and interrogated and insulted by Peisetaerus before being allowed to return back to Zeus. A third messenger arrives to say that men are flocking to the bird's newly formed city. One man arrives to Peisetaerus as he is inspired by the birds allowing permission to beat ones father, a right he would like to have. Next, Cinesias, the poet arrives, followed by a man that wishes to take advantage of having wings to prosecute those who he summons. This man is kicked out by Peisetaerus.
Next, Prometheus arrives, but hides his face so as not to be seen by Zeus. He has come to let Peisetaerus know that the gods are starving because the bird city is blocking all of the sacrifices from reaching them. Prometheus tells him that the gods want peace desperately, he tells Peisetaerus not to give up negotiating until he gets both Zeus' lightning bolt scepter and his princess, Sovereignty who is the real power of Zeus.
Prometheus leaves and Poseidon, Heracles and Triballians, an oafish god worshipped by barbarians arrive to negotiate peace with Peisetaerus. With Prometheus' advice in tow, Peisetaerus is able to get the three gods to concede to giving him Zeus' scepter and his princess. Peisetaerus is then married to the princess with Zeus' scepter in his hand.
