On a small island surrounded by water ('alazhars': dude an island IS a piece of land surrounded by water Duh!), a colony of ants is preparing food for the arrival of a band of grasshoppers. Of the ants that are working, one of them that stands out is an industrious one named Flik. Flik is constantly inventing new things for the colony to try, but his ideas are often shouted down and shunned by the colony. The only one who seems to believe in Flik is the young Princess of the colony named Dot. Secretly, Flik is attracted to her older sister, Atta, who is next in line for the throne.
As the time for the grasshoppers to arrive approach, the colony heads down into the anthill, intent to wait for the grasshoppers to eat the offering, and leave. Unfortunately, Flik is the last one to put his items on the offering stone, and ends up causing the platform to collapse with his piece of machinery.
When the grasshoppers finally arrive and find nothing, they go down into the anthill to terrorize the ants. The leader of the grasshoppers, demands that the offering be replenished by the Fall season, and terrorizes Dot, before Flik comes forward to try and defend her. Hopper then insists that the offering be doubled, due to Flik's speaking out at him. The grasshoppers then leave, promising to return when the last leaf falls.
The colony is now in trouble, as there isn't enough food to fulfill Hopper's request and provide sustenance for the colony. Flik is brought before a tribunal in regards to his causing the trouble. As the group convenes, Flik then thinks up a new idea: if the colony could get bigger bugs, they could be instrumental in scaring off the grasshoppers from ever returning to bully the colony. The others think this is a bad idea, until Flik volunteers to look. Thinking that his search will take a long time, the council decides to accept Flik's request, figuring he'll be away from them long enough to keep from causing further trouble.
Flik sets off the next day to head for the big city, eventually finding his way into a 'bug bar,' asking around for tough 'warrior bugs.' His attention is suddenly drawn to a group of bugs in a corner, who it seems are preparing to take on a much larger bug. However, in the fight, the 'bug bar' ends up being wrecked, and Flik misses much of the fight. However, in the aftermath, Flik thinks he's found the perfect guardians to help his colony.
He pleads his case to the group, saying how he's been looking for bugs with their talent, and asking for their help regarding the incoming group of grasshoppers. The group eagerly accepts, and they head off for Ant Island.
When Flik returns, Atta and the elders are shocked that Flik actually found 'warrior bugs.' Atta is at first unsure, but one of the group named Francis (Dennis Leary), promises that they will knock the grasshoppers 'dead' when they come.
A party is then held in honor of the group, including a tribute and art showing the warriors fighting off the grasshoppers. The group then grows leary, and it is then that a black widow spider of the group named rosie reveals to Flik through whispering, that they are not warrior bugs...but a group of out-of-work circus bugs!
Discovering their mutual misunderstanding, the circus bugs attempt to leave, but are forced back by a bird. They save Princess Dot, the Queen's daughter and Atta's sister, from the bird as they flee, gaining the ants' trust in the process. They continue the ruse of being "warriors" so the troupe can continue to enjoy the attention and hospitality of the ants. The bird encounter inspires Flik into creating an artificial bird to scare away Hopper, leader of the grasshoppers, who is deeply afraid of birds. The bird is constructed, but the circus bugs are exposed by their former ringmaster, P.T. Flea, when he arrives searching for them. Angered at Flik's deception, the ants exile him and desperately try to pull together enough food for a new offering to the grasshoppers, but fail to do so. When the grasshoppers discover a meager offering upon their arrival, they take control of the entire colony and begin eating the ants' winter store of food. After overhearing Hopper's plan to kill the queen, Dot leaves in search of Flik and convinces him to return and save the colony with his original plan. The plan nearly works, but P.T. Flea lights the bird model on fire, causing it to crash and be revealed as a fake. Hopper has Flik beaten in retaliation, but Flik defies Hopper and inspires the entire colony to stand up to the grasshoppers and drive them out of the colony.
Before Hopper can be disposed of, it begins to rain. In the chaos, Hopper viciously pursues Flik, who leads him to an actual bird's nest. Hopper mistakes the real bird for another fake bird, and taunts it, attracting its attention. The grasshopper is eaten by the bird and its chicks. Some time later, Flik has been welcomed back to the colony, and he and Atta are now a couple. As the troupe departs with the last grasshopper, Molt, as an employee, Atta is crowned the new Queen, while Dot gets the princess' crown. The circus troupe then departs as Flik, Atta and Dot watch and wave farewell in a tree branch.