After graduating Twilight traveled to Peru, New York, where he both taught class and studied for Congregational ministry. In 1826 Twilight married Mercy Ladd Merrill, a school teacher. He soon become the pastor of congregations in Vergennes, Vermont and also in Brownington. Upon returning to Vermont Twilight endeavored to open a school. He was not only the school's architect, but also its school master. Twilight's school was named Orleans County Grammar School. In order to garner needed students Twilight sought to raise funds and build the a granite public building, the first of its kind in Vermont. This building was predominately used as a dormitory named Athenian Hall.
Twilight was elected to Vermont's General Assembly in 1836. With this win he garnered another first, becoming the one African American to serve in a state legislature in the United States. Later, In 1847, after trouble with local school administrators and boards, Twilight decided to moved to Quebec. He was gone for five years, but returned to serve again as headmaster in a Brownington. Twilight died in June of 1857. He is buried in the Brownington churchyard near the historic Athenian Hall, which is now commonly referred to as the Old Stone House.
Today the public can visit the restored scene in the Northeast Kingdom village of Bloomington, Vermont to learn more about life in the 18th century, Alexander Twilight, his school, and African American history in Vermont. The museum is open Wednesday through Sunday most often from 11:00 am to 4:00 pm.