[1] It was established in 1642 to serve the Dutch inhabitants of Fort Orange, the adjacent village of Beverwyck, and the patroonship of Rensselaerswyck in general.

Theodore Roosevelt attended services here while Governor, and Queen Wilhelmina visited the church during its 300th anniversary year.

The terrain slopes very gently towards the Hudson River 1,000 ft (300 m) to the east, and more sharply upwards to the southwest and northwest, reflecting the ravine that gave the nearby Sheridan Hollow neighborhood its name.

The only contributing property to that district also listed individually on the Register, the Palace Theatre, is a block to the north, across Clinton (U.S. Route 9).

Across North Pearl is a small grassy traffic island separating Orange and the onramps to Interstate 787, which runs along the river.

[4] All windows on that facade, on the two stories of the towers and the larger one in the center of the main block, are stained glass, trimmed with stone.

The tripartite main entrance has a stone face and arcade of three round arches supported by smooth columns with Corinthian capitals.

[4] The two windows in the lower section of each tower are themselves slightly recessed in a round arch laid in splayed brick.

[4] The first stage of the towers has a slightly projecting central section, topped by a pediment, on each of its two outward faces, with a large clock in the center.

Corinthian columns support the ribbed vaulted ceilings, and a smaller arcade of five round arches with gilded tracery sets off the west wall of the chancel.

[4] After Henry Hudson explored the river that would be named after him in 1609, his employer, the Dutch government, began colonizing the valley as New Netherland.

The capital, Fort Orange, its boundaries roughly corresponding to Albany's present downtown, was established as far upriver as possible in order to strengthen the Dutch claim to the area.

[4] In 1624 the Dutch East India Company appointed someone to perform informal religious services for the settlers in the vicinity of the fort.

[5] Services were first held in the manor house of the local patroon, the Van Rensselaer family, then a converted warehouse and a log cabin.

[4] In 1656 the first dedicated church building, was built on the property of Jan Coster Van Auken adjoining his shop at what is now the steam boat landing, a stone structure was erected.

Worship continued unimpeded at the church, even as the Dutch briefly assumed control of the colony again during the Third Anglo-Dutch War.

[5] In 1782, as the war was ending with American independence a certain outcome, General George Washington visited the church's consistory to personally thank them for their support.

Around the same time, the church began holding its first services in English, which would totally overtake Dutch as its liturgical language within eight years.

Philip Hooker, a local carpenter's son who had been establishing himself as an architect in the Albany area, was commissioned to design it.

It took several years to get construction going on Hooker's first major work, delayed by punch list items like changing the roof cladding from shingles to copper and altering the cupola design.

In 1798, a few months before the $25,000 ($449,000 in modern dollars[7]) project was completed and opened for services, one of Albany's newspapers called it "a superb and elegant building.

The sanctuary was repainted, a dark red oak reredos installed in the chancel, and the choir loft widened.

In 1973, after changes in the RCA's Book of Church Order permitted it, the first female elder and deacon were elected.

The next year Clee Park was dedicated as the church marked its National Register listing, and summer drive-in worship, in which attendees remain in their cars while the minister conducts services from an outdoor pulpit,[10] began.