It is in the Chapel that the University comes together as a community. This is true at Opening Exercises, Baccalaureate Services, and annual memorial services for alumni and staff of the University. It has also been a bridge between town and gown, and between the several academic communities of Princeton.

The present University chapel was designed by Ralph Adams Cram of Boston. Cram, a leading architect of Gothic revival, was supervising architect of the University at the time and also designed the Graduate College. Built between 1925 and 1928 at a cost of $2,500,000, the University chapel is one of the largest college chapels in the world.

At its founding in 1746 the College of New Jersey was first located in the parsonage of the Presbyterian Church of Elizabeth and soon afterwards in a sister church in Newark. When the College moved to Princeton in 1756, the chapel was located in what eventually became the Faculty Room in Nassau Hall. This arrangement lasted until 1847,when a separate building was constructed on the site of East Pyne. However, by the end of the Civil War a new chapel was needed because the number of undergraduates had doubled. Henry Gurdon Marquand, a founder of the Metropolitan Museum of Art, was the principal donor for the Marquand Chapel, which was built in 1881. This chapel was destroyed by fire during house party weekend in 1920, and, for several years, worship services were held in Alexander Hall, the place where Professor Woodrow Wilson had delivered his address "Princeton in the Nation's Service."

Many Princetonians are remembered in the Chapel's stained-glass windows and in engravings on the pews, on memorial stones on the walls, in the silver communion chalices, memorial hymnals, and on many of the furnishings. John Witherspoon, sixth president of the College and the only clergyman to sign the Declaration of Independence, is pictured in the Great South Window (Christ the Teacher). The figure of James Madison, Witherspoon's student, is in the Window of the Law, high up in the south clerestory near the entrance of the chapel.

The oak pews in the nave are made from wood originally intended for Civil War gun carriages. The magnificent pulpit, brought from France, probably dates back to the mid-16th century and had been painted bright red prior to its installation in this chapel. The wood for the pews in the chancel, where the choir and clergy are seated for services, came from Sherwood Forest in England and took 100 people over a year to carve. The statues adorning these pews represent figures in the history of music, scholars, and teachers of the church. In the center of the chancel is the Great East Window (The Love of Christ). The chancel is flanked by six bays of windows, the first two representing two psalms of David, and the remaining windows depicting cycles from four great Christian epics: Dante's Comedia, Malory's Le Morte d'Arthur, Milton's Paradise Lost, and Bunyan's Pilgrim's Progress. The Chapel is also decorated with 25-foot silk paintings by Juanita Y. Kauffman. The Threshold paintings were commissioned for the University's 250th anniversary, and the Ascent: Blue River paintings were commissioned for and unveiled during the Pentecost of 1999.

The present organ is the result of a renovation in 1991 by N. P. Mander Ltd. of England, creating a magnificent instrument in the English cathedral style that is especially well-suited to the grandeur of the Chapel, featuring 109 stops and 8,000 pipes.

The University formally opens and closes the academic year with an interfaith service in the chapel. An ecumenical Christian service, led by the dean of the chapel, is held on Sunday mornings. Several Christian denominations, including Catholic, Baptist, Lutheran, and Episcopal, also worship there regularly. The chapel is the site of special services of music, thanksgiving, and penitence, as well as weddings, baptisms, and funerals. In addition, each year a service of commemoration is held for members of the campus community and alumni. On certain extraordinary occasions, the chapel has been chosen as the gathering place for the entire campus.