Melanie Daniels (Tippi Hedren), a young socialite known for rather racy behavior and playing pranks, meets lawyer Mitch Brenner (Rod Taylor) in a San Francisco bird shop. He wants to purchase a pair of lovebirds for his sister's eleventh birthday, but the shop has none. He had seen her in court once before when her recklessness resulted in the breaking of a plate-glass window, but she does not know him; attracted, he plays a prank by pretending to mistake her for a salesperson. She is infuriated when she discovers this, even though she also likes to play practical jokes. Then, intrigued by his veiled advance, she finds his weekend address in Bodega Bay, purchases a pair of lovebirds, and makes the long drive to deliver them. Discovering he is not there, she leaves the birdcage inside the Brenner family home, with a note. He spots her on the water through a pair of binoculars during her retreat, and races across the bay to head her off. She is attacked near shore on the town side and injured by a seagull. He invites her to dinner, and she hesitantly agrees.
Melanie gets to know Mitch, his alternately domineering and needy mother Lydia (Jessica Tandy), and his younger sister Cathy (Veronica Cartwright). She also befriends local schoolteacher Annie Hayworth (Suzanne Pleshette), Mitch's ex-lover. When she spends the night at Annie's house they are startled by a loud thud; a gull has killed itself by flying into the front door. At Cathy's birthday party the next day, the guests are set upon by seagulls. The following evening, sparrows invade the Brenner home through the chimney. The next morning, Lydia, a widow who still sees to the family farmstead, pays a visit to a neighboring farmer to discuss the unusual behavior of her chickens. Finding his eyeless corpse pecked lifeless by birds, she flees in terror. After being comforted by Melanie and Mitch, she expresses concern for Cathy's safety at school. Melanie drives there and waits for class to end, unaware that a large murder of crows are massing in the nearby playground. Unnerved when she sees its jungle gym covered by them, she warns Annie, and they evacuate the children. The commotion stirs the crows into attacking, injuring several of the children. A young girl is seriously injured after being felled by the crows, her eyeglasses shattering. She calls on Cathy for help and Melanie pushes them into a parked car, blasting the horn as crows engulf the vehicle.
Melanie calls her father's newspaper from The Tides restaurant. Several patrons describe their own encounters with aggressive bird behavior. An amateur ornithologist dismisses the reports as fanciful and argues with Melanie over them. Mitch arrives with the sheriff and corroborates Melanie's claims. As the patrons argue about the likelihood of such ornithological behavior, Melanie notices birds swooping at a man across at the gas station. She alerts the others and they witness the man knocked unconscious while filling a car with fuel, which spills out onto the street. As the patrons run outside to assist, unaware of the danger, a bystander attempts to light a cigar, igniting a pool of gas and becoming incinerated. The explosion attracts a mass of gulls, which begin to swarm menacingly as townsfolk attempt to tackle the fire. Masses of birds launch an attack, causing serious injury and traffic collisions. Melanie is forced to take refuge in a phone booth, which is pummeled by birds, shattering the glass. We see her point of view as the town descends into chaos – a horse and cart topples its load as crows ravage the horses, an out-of-control car crashes into the burning vehicles as the driver is attacked by gulls, a bloodied man staggers helplessly against the phone booth doors as he is ravaged. Melanie is eventually rescued by Mitch and they return to the restaurant, where Melanie is accused of causing the attacks, which began with her arrival. Melanie slaps the increasingly hysterical mother, shocking her back to reality. During a lull in the bird attacks, Mitch and Melanie return to Annie's house and find that she has been killed by the crows while ushering Cathy to safety.
Melanie and the Brenners seek refuge inside the family home. Mitch and Melanie work together, Melanie handing planks up to Mitch, who nails the planks over the windows. That night, the home is attacked by waves of birds, injuring Mitch's hand and arm. During a nighttime lull between attacks, Melanie hears the sound of fluttering wings; not wanting to disturb the others' sleep, she enters the kitchen and sees that the lovebirds are sedentary. The sounds are emanating from above. She cautiously climbs the staircase and enters the first bedroom, where she sees that the birds have broken through the roof. They violently attack her, trapping her in the room until Mitch comes to her rescue. She is badly injured and in shock. Mitch insists they must get her to the hospital, suggesting they drive to San Francisco despite the risk. The radio reports the spread of bird attacks to nearby communities, and suggests that the military may be required to intervene because civil authorities are unable to cope. Reports are that most Bodega Bay residents have fled the community. When Mitch looks outside, it is dawn and a sea of birds ripples menacingly around the Brenner house as he prepares Melanie's car for their escape. Lydia cradles Melanie in the backseat, where the camera captures a child-like look of gratitude on Melanie's face as she gazes up into the now-maternal visage of Mitch's mother Lydia. In the final shot, the car carrying Melanie, Mitch, Lydia, Cathy, and the lovebirds slowly makes its way through a landscape in which thousands of birds perch ominously.