Brenneker is a lyre spider, a musical one, who used to live in a forest, inside a tree, but her wood was cut down to be made into a lute one day, and so she ends up living inside of the instrument. The lute is bought by a girl named Laurel, who takes the instrument after playing it in the shop and being surprised (as was the instrument's maker) by the lovely tones created by Brenneker's harmonizing on her musical web.
Laurel takes lessons from the lute maker, and when she improves, Brenneker rewards her by harmonizing with her, creating wonderfully rich tones. The lute maker seems to know what is going on, and advises Laurel to leave a window open with a bowl of milk and honey for her fairy harpist in the lute, which actually does attract flies and insects for Brenneker's meals. The only sadness in Brenneker's life is her loneliness, as no spiders like her seem to exist where she is, and no one answers her mating call.
Her loneliness is further exacerbated when Laurel finds a lover, a recorder player named Thomas. The two are happy together, but one night they have an argument. That night, Brenneker hears the sound of another lyre spider, and answers with her own music. The spider, named Wisterness, comes to her lute, and they talk for a time, but it is not mating season, so he leaves and they play to each other that night. Laurel argues with Thomas about their future further, as she wants to go to university to pursue music. She takes on students, saving the money from lessons for university. Brenneker and Wisterness try to consummate their love, but Brenneker is now too large to fit through the small holes in the instrument, and is now trapped inside.
Laurel decides to enter a music scholarship competition, and asks Thomas if he will support her and come with her to the city to be together while she is at university, but he cannot, so they breakup. Brenneker is preoccupied by Laurel's sadness, but then finds herself distracted by a larger problem—a woodworm has begun to destroy the lute from the inside. She just misses killing it, and it continues to eat away at the spruce wood, leaving Brenneker no option other than to patch up the holes with her webbing.
Laurel is advised to play a duet for the competition, but she has no way to find a duet partner with Thomas refusing to help her. She goes to the competition alone, with Brenneker frantically patching holes created by the woodworm, spending her own energy. With Brenneker's accompaniment, Laurel is chosen to be a finalist, and in her finals performance, Brenneker breaks from her traditional harmonizing role and plays the counterpoint harmony to the song that should've been a duet, giving the impression that Laurel is playing a two part duet on her one instrument.
When Laurel wins the competition and is called to play an encore, the weakened instrument finally snaps, exposing the weakened Brenneker to Laurel, who recognizes that she has been the one to bring such lovely life to the instrument. Laurel feeds Brenneker for a few days, then sets her free in the woods back home. Brenneker reunites with Wisterness, and they mate, after which Brenneker eats Wisterness, as spiders do. When Brenneker's children float away on their own weeks later, she is finally not alone.