Culler attended Harvard for his undergraduate studies, where he received a Bachelor of Arts in history and literature in 1966. After receiving a Rhodes scholarship, he attended St. John's College, Oxford University, where he earned a B. Phil in comparative literature (1968) and a D.Phil in modern languages (1972). His thesis for the B. Phil., on phenomenology and literary criticism, recorded Culler's first experiences with structuralism. The thesis explored the work of Maurice Merleau-Ponty and the criticism of the "Geneva School". using the ideas of Claude Lévi-Strauss, Roland Barthes, and Ferdinand de Saussure. His D. Phil. thesis, "Structuralism: A Study in the Development of Linguistic Models and their Application to Literary Studies", formed the basis of his later prize-winning book, Structuralist Poetics. By the mid-1970s, Jonathan Culler became the voice of structuralism in America.
Culler was Fellow in French and Director of Studies in Modern Languages at Selwyn College, Cambridge University, from 1969-1974, and Fellow of Brasenose College, Oxford and University Lecturer in French from 1974-77. He was Visiting Professor of French and Comparative Literature at Yale University in 1975. He is a past president of the Semiotic Society of America (1988).
Inspired by the monumental linguistic theories of Ferdinand de Saussure and the methodological essays of Claude Lévi-Strauss, Culler wrote Structuralist Poetics: Structuralism, Linguistics and the Study of Literature, which won the James Russell Lowell Prize from the Modern Language Association of America in 1976 for being an outstanding book of criticism. Structuralist Poetics was one of the first introductions to the French structuralist movement in English.
Culler’s contribution to the Very Short Introductions series, Literary Theory: A Very Short Introduction, has received praise for its innovative technique of organization. Rather than dedicate chapters to schools and their methods, he divides into eight chapters the issues and problems that literary theory approaches.
In a book recently published in 2007, The Literary in Theory, Culler responds to the greater notion of Theory and the history of literature’s role in the larger realm of literary and cultural theory. He defines Theory as an interdisciplinary body of work including structuralist linguistics, anthropology, Marxism, semiotics, psychoanalysis, and literary criticism.
Culler proposes that he can provide a more thorough account of the use of linguistics in structuralism than his predecessors. The linguistic model can help “formulate the rules of particular systems of convention rather than simply affirm their existence". He posits that language and human culture operate in similar ways. In Structuralist Poetics, however, Culler warns against the error of applying the technique of linguistics directly to literature. Rather, the "'grammar' of literature" is converted into literary structures and meaning within a competent reader. He defines structuralism as a theory which rests on the realization that if human actions or productions have meaning there must be an underlying system which makes this meaning possible. An utterance has meaning only in the context of a preexistent system of rules and conventions.
Culler proposes that we use literary theory not necessarily to try to understand a text but rather to investigate the activity of interpretation. We should give more weight to the active participation of the reader. In several of his works, he speaks of a reader who is particularly "competent". In order to understand how we make sense of a text, Culler intends to identify common elements that all readers immediately treat differently in different texts. He suggests there are two classes of readers, “the readers as field of experience for the critic (himself a reader)” and the future readers who will benefit from the work the critic and previous readers have done. Critics of Culler’s theories cite his lack of distinction between literature and the institution of writing in general.