In 1930s Edinburgh, six 10-year-old girls, Sandy, Rose, Mary, Jenny, Monica, and Eunice, are assigned Miss Jean Brodie, who describes herself as being "in [her] prime," as their teacher.

Miss Brodie, determined that they shall receive an education in the original sense of the Latin verb educere, "to lead out", gives her students lessons about her personal love life and travels, promoting art history, classical studies, and fascism.

In the Junior School, they meet the singing teacher, the short Mr. Gordon Lowther, and the art master, the handsome, one-armed war veteran Mr. Teddy Lloyd, a married Catholic with six children.

However, Miss Brodie never overtly acts on her love for Mr. Lloyd except once to exchange a kiss with him, witnessed by Monica.

During a two-week absence from school, Miss Brodie embarks on an affair with Mr. Lowther on the grounds that a bachelor makes a more respectable paramour: She has renounced Mr. Lloyd as he is married.

At one point during these two years in the Junior School, Jenny is "accosted by a man joyfully exposing himself beside the Water of Leith.

[4] Once the girls are promoted to the Senior School (around age 12) but now dispersed, they hold on to their identity as the Brodie set.

All the while, the headmistress Miss Mackay tries to break them up and compile information gleaned from them into sufficient cause for Brodie's dismissal.

Miss Brodie takes her under her wing separately, encouraging her to run away to fight in the Spanish Civil War on the Nationalist side, which she does, only to be killed in an accident when the train she is travelling in is attacked.

Sandy, with a keen interest in psychology, is fascinated by Mr. Lloyd's stubborn love, his painter's mind, and his religion.

Rose, however, is oblivious to the plan crafted for her, and so it is Sandy, now 18 and alone with Mr. Lloyd in his house while his wife and children are on holiday, who has exactly such an affair with him for five weeks during the summer.

Not until her dying moment a year after the end of World War II is Miss Brodie able to imagine that it was Sandy who betrayed her.

Again unlike Sandy, Rose "shook off Miss Brodie's influence as a dog shakes pond-water from its coat.

Jean Brodie is genuinely intent on opening up her girls' lives, on heightening their awareness of themselves and their world, and on breaking free of restrictive, conventional ways of thinking, feeling, and being".

"[13] The character of Miss Jean Brodie was based in part on Christina Kay, a teacher of Spark's for two years at James Gillespie's School for Girls.

Spark later wrote of her: "What filled our minds with wonder and made Christina Kay so memorable was the personal drama and poetry within which everything in her classroom happened.

[15] Jay Presson Allen's adaptation of the novel was staged at the Brunton Theatre, Musselburgh, under the direction of Charles Nowosielski, in October 1987, with Beth Robens in the title role.

[16] On 5 November 2019, The Prime of Miss Jean Brodie appeared on the BBC News list of the 100 most influential novels.