Ant Island is a colony of ants led by the Queen and her daughter, Princess Atta.
Every season, they are forced to give food to a gang of marauding grasshoppers led by Hopper.
One day, when Flik, an individualist and would-be inventor, inadvertently knocks the offering into a stream with his latest invention, a grain harvesting device, Hopper demands twice as much food as compensation.
When Flik suggests in earnest that they seek help from other stronger bugs, the other ants see it as an opportunity to remove him and send him off.
At the "bug city", which is a heap of trash under a trailer, Flik mistakes a troupe of Circus Bugs (who were recently dismissed by their greedy ringmaster, P.T. Flea) for the warrior bugs he seeks.
The bugs, in turn, mistake Flik for a talent agent, and accept his offer to travel with him back to Ant Island.
During a welcome ceremony upon their arrival, the Circus Bugs and Flik both discover their mutual misunderstandings.
The Circus Bugs attempt to leave, but are attacked by a bird; while fleeing, they save Dot, Atta's younger sister, gaining the ants' respect in the process.
At Flik's request, they continue the ruse of being "warriors", so the troupe can continue to enjoy the hospitality of the ants.
Hearing that Hopper fears birds inspires Flik to create a false bird to scare away the grasshoppers.
Meanwhile, Hopper tells his gang how greatly the ants outnumber them and worries that they will eventually rebel against them.
The ants finish constructing the fake bird, but during a celebration, P.T. Flea arrives, searching for his troupe, and inadvertently reveals their secret.
Outraged by Flik's deception, the ants exile him, and desperately attempt to gather food for a new offering to the grasshoppers.
However, when Hopper returns to discover the mediocre offering, he takes over the island, and demands the ants' winter food supply, planning to assassinate the Queen afterwards.
Overhearing the plan, Dot goes after Flik and the Circus Bugs to inform them, convincing them to return to Ant Island.
After the Circus Bugs distract the grasshoppers long enough to rescue the Queen, Flik deploys the bird; it initially fools the grasshoppers, but P.T. Flea, who also mistakes it for a real bird, burns it, exposing it as a decoy.
Hopper beats Flik in retaliation, saying that the ants are humble and lowly life forms who live to serve the grasshoppers.
However, Flik responds that Hopper actually fears the colony, because he has always known what they are capable of, inspiring the ants and the Circus Bugs to fight back against the grasshoppers.
The ants attempt to force Hopper out of Ant Island using P.T. Flea's circus cannon, but it suddenly begins to rain. In the ensuing chaos, Hopper frees himself from the cannon, and abducts Flik.
After the Circus Bugs fail to catch them, Atta rescues Flik. As Hopper pursues them, Flik lures him to the nest of the bird he, Dot, and the Circus Bugs encountered earlier.
Thinking that the bird is another decoy, Hopper taunts it before discovering in panic that it is real, and is captured and devoured by its chicks.
With their enemies gone, Flik has improved his inventions along with the quality of life for Ant Island, he and Atta become a couple, and they give Hopper's younger brother Molt, and a few ants to P.T. Flea as new members of his troupe.
Atta and Dot respectively become the new queen and princess.
The ants congratulate Flik as a hero, and bid a fond farewell to the circus troupe, who promise to return in the future.