Jami Masjid is the principal building of Fatehpur and the vastest, spanning 133.6 metres north to south and 165.2 metres east to west. According to inscriptions on either side of the central archway of the prayer chamber, the construction of the mosque was completed in 1571-72.

Akbar acknowledged his deep gratitude and respect for Shaikh Salim Chishti by ascribing the mosque to him. The Shaikh died on 14 February 1572 aged 95 lunar years (92 solar years) and the great mosque must have been nearly complete before his death. Legend has it that the emperor himself often swept the floor of the mosque and called the azan. In 1579, he read the khutba, the prayer to proclaim his sovereignty, and also issued the mahzar or declaration from the hallowed precincts of Jami Masjid that assigned to him unlimited powers in religious matters. Although conceived on a scale larger than any previous mosque in India, the Jami Masjid follows the conventional structure of a mosque - it comprises an open courtyard with pillared cloisters on three sides and the western end occupied by the sanctuary.

The prayer hall has an arcade of pointed arches, interrupted and dwarfed by a towering central iwan which tends to obscure the central dome, while the lateral domes lurk behind a fringe of chhattris.

There are three mihrabs (marking the direction of the holy city of Mecca), in each of the seven bays. The central mihrab of Jami Masjid, pentagonal in shape and covered by a semi-dome, is a splendid specimen of traditional decorative art.

To the right is the minbar, a simple marble structure of three steps, from where was read the Friday oration or the khutba. Special orations were also read on the occasion of Id-ul-Qurban and Id-ul-Fitr, the two great festivals of the Muslim calendar.

From either side of the central chamber, one can pass into the north and south aisles through three arched openings. The wings are divided into three halls, each provided with a central mihrab flanked by two smaller ones, embellished with Quranic verses.

The flat roofs of the side halls are supported on corbels rather than squinches. Akbar seems to have absorbed this architectural style from Gujarat after his conquest of that region. This deliberate use of Hindu structural forms in a mosque had not been paralleled in northern India for 300 years, since the early days of the Muslim advent produced structures such as the Quwwat-ul-lslam Masjid next to Qutub Minar in Delhi or the Adhai Din ka Jhonpra in Ajmer.