Virgil's earliest critics concentrated on discussing the style in which he wrote and the sources from which he drew his material. The Aeneid was written for a cultured and educated, extremely well-read audience, and almost immediately became a school text. Many Roman critics wrote treatises explaining the book's historical, religious, philosophical, and literary allusions to make it easier for teachers and students alike to understand. Others wrote explanations of difficult words or unusual grammar. In the fourth century, a teacher named Donatus published excerpts from many of these works to produce a kind of general reader's guide. A generation later, another teacher, Servius, relying in part on Donatus, produced a similar commentary for schools.

Macrobius's Saturnalia written in the first half of the fifth century, treated Virgil as a Roman bible. Macrobius depicted actual historical figures, including Servius, discussing the Aeneid. These figures were members of the last generation of educated Roman pagans, attempting to defend their gods, their way of life, the very nature of Rome, from the growing cult of Christianity.

Early Christian reaction to Virgil was mixed. On one hand, he was the poet of the Roman state and religion, which Christianity sought to usurp. On the other hand, his work was an essential part of a complete education, and he was widely considered the finest poet writing in Latin. Christian poets like Prudentius used Virgil as a model. Saint Augustine of Hippo admitted crying over Dido's tragic end when he read the Aeneid as a schoolboy. In the end, western Christianity simply co-opted Virgil. In his Fourth Eclogue Virgil had written about the birth of a wonderful child who would end war and bring back the golden age. For this, Virgil was popularly (if not officially) accepted as a prophet of Christ.

During the early middle ages, the Aeneid was used as a schoolbook for the study of Latin. Servius's commentary, with or without extra material from Donatus, was reprinted many times. In the late fifth or early sixth century, a Christian wrote a short treatise in the form of a rather humorous vision of Virgil in which the poet explained the Aeneid as an allegory—an extended narrative metaphor—about the soul's growth to maturity and virtue. From the late eleventh century on, Virgil's reputation for enormous learning, a few allegorical passages in Servius, and the popularity of allegory as a literary form changed the way people read the Aeneid. It was often treated as a sort of coded message, full of deep, hidden meanings. This approach was popular until the time of Shakespeare. It had a big impact on how other epic works were written. Writers like Torquato Tasso or Edmund Spenser wrote epics according to this allegorical model, with the action and even characters all serving as metaphors or symbols for something else. Throughout all the changes in literary and critical fashion, the Aeneid remained popular simply as a story. The earliest French romance was not about Lancelot and Guinevier, but Aeneas and Lavinia.

Modern criticism of the Aeneid began in the seventeenth century. Late seventeenth- and early eighteenth-century French and English critics began to interpret the Aeneid not as an allegory, but as a narrative which conveyed meaning in the same way as history. The narrative provided models of the highest qualities of conduct for both princes and their subjects. In the dedication to his translation, the poet John Dryden stressed these elements, which appealed to the readers of his time, who were looking for royal leadership into an era of national renewal.

Proponents of literary Romanticism in the late eighteenth- and early nineteenth centuries reacted against the classicism of the 1600s and 1700s, when Greek and Latin texts from Virgil's era were highly praised and imitated. The Romantics found Aeneas a poor hero and were not impressed with Roman destiny as a theme. When they praised Virgil at all, they did so for his style or for the same emotional sensitivities they admired in their own poetry. This approach lead readers to examine what critics have come to call Virgil's "private voice." For much of the nineteenth century, Romantic critics and commentators focused on examining Virgil's treatment of individual human beings caught up in the larger issues of Rome's destiny.

In the twentieth century, criticism of the Aeneid has become increasingly more sophisticated in its understanding of the literary, social, and political realities of Virgil's world. Modern critics still reflect as much of their own world as of Virgil's. Two world wars and the end of colonialism have affected reader responses to the events depicted in the work. A critical arena which has shown great development is the continuing study of readers' changing attitudes about Virgil over the centuries. Kenneth Quinn's observation that Virgil "is rarely completely for a character or completely against the character opposing him" is one of the most important ideas that any reader can bring to the Aeneid.