The chapel was designed by prominent traditionalist architect Duncan G. Stroik in a neoclassical style intended to evoke the work of Christopher Wren and early Georgian churches in the United States.

[3] However, amid Hillsdale's growth in attendance, President Larry P. Arnn saw a need for an ecumenical space for worship on campus, saying at the time that "[t]here has never been a great university that was not heavily concerned with the question of God.

"[10] The chapel would need to facilitate worship for both Hillsdale's Protestant majority and its substantial minority, roughly 30 percent, of Roman Catholics.

[13]Other guests at the dedication included Hillsdale College board chairman Pat Sajak and journalist Mollie Hemingway.

[15] As of the summer of 2024, the chapel is open daily and used for regular campus worship events, including a new choral evensong service envisioned by Arnn.

In July 2024, the chapel was filled to capacity for the funeral services for Hillsdale County sheriff's deputy Bill Butler Jr., who had been killed by a driver during a routine traffic stop.

The tholos is formed by eight Doric limestone columns, and the dome inside the portico is made of self-supporting red brick and spans 32 feet.

[22] In the portico, three convex entrance doors are marked with roundels, each made of different-colored marble, featuring the Latin names of the three theological virtues: Fides (faith), Spes (hope) and Caritas (charity).

[3] The marble narthex features symbols of Christianity: the Ark of the Covenant, the Chi Rho, the Trinity and a dove representing the Holy Spirit.

"It was an interesting tension to have a place of worship also function as a state-of-the-art musical performance hall," Stroik said, "because my view of sacred space is to set it apart and not have it be used for profane purposes.

"[3] At the top of the ten arches separating the columns are gold-leaf escutcheons bearing names of the fruits of the Holy Spirit in Latin.

[1] The chancel features a mahogany pulpit and sounding board, a lectern, an organ designed for choral accompaniment, and enough space for Hillsdale's 100-voice choir and chamber ensemble.

"[23] Commentator Dennis Lennox remarked on how the interior evokes the Anglican churches of Wren and Nicholas Hawksmoor while its liturgical west front "looks very Roman Catholic.

"That Christ Chapel should have been designed by a Catholic but in a mostly Anglican or Protestant register indicates something of the ecumenical spirit that Hillsdale aims to foster," he wrote.

"President Arnn sees the building as a 'mere Christian' kind of space, a place where the different spiritual traditions present among the student body (and indeed among the faculty) can all feel welcome, where commonalities can be celebrated and Balkanization avoided."

Kimball commented that "[w]hen you walk into Christ Chapel, you catch your breath in response to the soaring grandeur of the space.

'"[5] For his work on Christ Chapel, Stroik was recognized with a 2021 Palladio Award for a design of less than 30,000 square feet from the Traditional Building Conference.