Plot

A colony of ants, led by the elderly Queen (Phyllis Diller) and her daughter Princess Atta (Julia Louis-Dreyfus), live in the middle of a seasonally dry creek bed on a small hill known as "Ant Island". Dot is Atta's sister. Every summer, they are forced to give food to a gang of grasshoppers, led by Hopper (Kevin Spacey). The food is placed in a heap on a precariously placed rock on the edge of the hill. Mr. Soil (Roddy McDowall) is the ant colony's resident thespian who helps ensure that the food collection lines continue to function without interruptions.

Flik (Dave Foley) is a courageous but clumsy inventor ant. Flik is constantly inventing new things for the colony to reduce labor, but his ideas are often shouted down and shunned by the colony, who feel the old-fashioned way of preparing the grasshoppers' "offering" is the only way to do things. Secretly, Flik is attracted to her older sister, Atta, who is next in line for the throne. The only one who seems to believe in Flik is the young Princess of the colony named Dot. Flik was always encouraging to Dot and says that in her is the potential for a future Queen and that she should never give up.

Flik inadvertently destroys the food offering with his grain harvester (which he claimed would have sped up harvesting and ensured that the ants save enough for themselves after making an offering to the Grasshoppers). Flik was placing the last harvested food on the offering pile when his machine knocks over one of the stones holding up the offering rock. The food heap is knocked off the hill and falls into the water at the bottom of the hill. Flik was the last one to put his food on the offering stone, while the rest of the ants were inside the anthill waiting for the grasshoppers to collect and offering and leave.

When the grasshoppers finally arrive and find nothing, they break into the anthill to terrorize the ants. The leader of the grasshoppers, Hopper, demands that the offering be replenished by the Fall season, and terrorizes Dot Flik comes forward to try and defend her. Hopper then commands that the offering be doubled due to Flik's standing up against them. Hopper promises to return at the end of the season when the last leaf falls. During the meeting, Hopper's dimwitted brother, Molt, lets it slip that Hopper is afraid of birds.

The Queen is distraught as the ants needed this time to collect food for themselves. Now the ants have to choose between a battle with the grasshoppers and starvation in the winter. Flik is brought before a tribunal in regard to his causing the trouble. Flik earnestly suggests the ants enlist the help of bigger bugs to fight the grasshoppers. The others think this is a bad idea, until Flik volunteers to look. Atta sees it as a way to get rid of Flik (so that he cannot mess anything up) and sends him off. Leaving the Island is considered a suicide mission by the ants.

Flik travels to "the city", which is essentially a heap of trash under a trailer. A motley crew of bugs are performing in a circus led by a flea, PT Flea. The circus isn't well-attended, most of the audience being flies who jeer and cajole the performers, especially when their acts fail. PT, desperate to keep the flies from leaving, announces a new act call "Flaming Death" where his crew will work together to keep him from being burned. The act fails miserably because the bugs can't coordinate their efforts and PT is burned anyway. He fires them all on the spot. The bugs were at a tavern when Francis, the ladybug is harassed by 2 insects from their earlier show. Francis and the fellow bugs stand up to the insects including small gang of flies and their huge member, Thud, forcing them to withdraw. Flik was at the "bug bar" but is pushed back by the crowd and cannot see the bugs running away from the insects. 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, thinking Flik wants them to perform at a dinner theatre and, hoping to avoid trouble from the bar's owner & the flies they fought with, they head off for Ant Island.

The bugs include Slim (David Hyde Pierce) a stick bug clown who often becomes a stand-in for stick-like props, Heimlich (Joe Ranft) a gluttonous, German-accented green caterpillar clown who desires to be a butterfly, Francis (Denis Leary) a hot-tempered male ladybug clown who is frequently mistaken for a female, Manny (Jonathan Harris) an elderly, English-accented praying mantis magician, Gypsy (Madeline Kahn) a moth who is Manny's wife, and his lovely assistant, Rosie (Bonnie Hunt) a black widow spider, Tuck and Roll (Michael McShane) twin pill bug performers from Hungary who speak in gibberish and act as cannonballs and dancers and Dim (Brad Garrett) a blue childlike rhinoceros beetle that plays the "ferocious beast". The bugs fly over the dry creek bed and reach Ant Island with Flik. The bugs believe that they have to "perform" their entertainment act for the visiting grasshoppers.

During a welcome ceremony after their arrival (Princess Atta is very impressed with Flik for actually returning with fearsome looking bugs), the Circus Bugs and Flik discover their mutual misunderstandings. When the ant kids present a mural in honor of the bugs, they realize that they are supposed to fight the grasshoppers away. Rosie tells Flik that they are circus performers and not warriors as assumed by the ants. Rosie whispers to Flik that they're actually just circus bugs and Flik is horrified, accusing the group of tricking them. When Atta appears, Flik convinces her that the circus bugs will fight for them.

The Circus Bugs attempt to leave. Flik begs them to stay as he knows that he will be branded with this mistake for the rest of his life in the colony. Princess Atta could already sense that something was wrong and had followed Flik with the Queen. While fleeing, they rescue Atta's younger sister Dot (Hayden Panettiere) from a bird who had found the insects, thereby gaining the ants' respect as Atta and the Queen were watching from the hill. The bugs work together to distract the bird while they rescue Dot and bring her back to safety on the Island.

Francis was injured while fighting the bird and saving Dot. As an honor to him, the Blueberry Scouts (a group of child ants of which Dot is a member) nominates Francis to be their "Den Mother". At Flik's request, the Circus Bugs continue the ruse of being "warriors", thus enabling them to continue enjoying the ants' hospitality. Princess Atta confides her own insecurities with Flik and says that she feels that everybody is just waiting for her to make a mistake.

Learning that Hopper fears birds inspires Flik to build a crewed Ornithopter disguised as a bird to scare away the grasshoppers. Atta likes the idea when communicated to her by the warriors and she commits the whole colony to build the device. The bird is constructed from sticks and leaves. Meanwhile, the grasshoppers don't want to return to Ant Island as they don't even like grain. Hopper reminds his gang of the ants' superior numbers, warning them the ants will rebel if not kept in line. Hopper says that the ants outnumber them by 100 to 1.

Meanwhile, building the fake bird brings the whole colony together and the ants are in a festive mood. Princess Atta thanks the bugs and Flik for bringing about this change. The ants finish constructing the fake bird. During the subsequent celebration, the Circus Bugs' old supervisor, P.T. Flea (John Ratzenberger), arrives, seeking to rehire them and blowing their cover; the ants exile Flik and the Circus Bugs, and desperately try gathering food for a new offering. The situation is hopeless as the last leaf is about to fall and the ants did not gather any food for the grasshoppers as they were busy building the fake bird.

Hopper returns, sees the mediocre offering, and takes over the island. He then demands the ants' own winter food supply, planning to execute the Queen afterward. Overhearing the plan, Dot persuades Flik and the Circus Bugs to return to Ant Island. Flik was demoralized and believed that the fake bird would not work. The bugs remind Flik that he was the one who found them, and his efforts brought the colony together to build the fake bird as well.

Flik and the bugs find that Hopper has rounded up all the ants and has taken away all of the colony's collected food supply. After the Circus Bugs distract the grasshoppers long enough (with their Circus act) to rescue the Queen, Flik deploys the bird. It initially fools the grasshoppers, but P.T., who is also fooled, sets the bird on fire. Realizing the deception, Hopper captures Dot and finds out that the fake bird was Flik's idea. Hopper has Flik publicly beaten (who reveals that he knew Hopper's plan to kill the Queen after the food was taken from the colony) and proclaims the ants are lowly life forms who live only to serve the grasshoppers. Flik asserts Hopper actually fears the colony, because he has always known what they are capable of. This inspires the ants and the Circus Bugs to fight back against the grasshoppers, driving all but Hopper and his brother Molt (Richard Kind) away.

The ants shove Hopper into the circus cannon to shoot him off of the island, but rain suddenly begins to fall. In the ensuing chaos, Hopper frees himself from the cannon and abducts Flik. The Circus Bugs and Atta pursue, with the latter catching up to Hopper and rescuing Flik, who lures Hopper to the real bird's nest. Hopper threatens to gather more grasshoppers and return the following seasons to annihilate the ant colony. Believing the bird is another fake, Hopper taunts it, until it grabs him and feeds him to its chicks.

With the anthill now at peace, Flik improves his inventions to help gather food for the ants. Flik and Atta become a couple and proceed to send Hopper's affable brother Molt and a few ants to help P.T. and the Circus Bugs on their new tour. Atta and Dot become the new Queen and Princess. The ants celebrate their victory and congratulate Flik as a hero. They then bid a fond farewell to the circus troupe.