Vermont's second State House, designed by Ammi Young, was completed in 1838 at a cost of $132,000. With a front portico modeled after the temple of Theseus in Greece, this classically-inspired building displayed a low saucer-shaped Roman dome and was the perfect embodiment of the chaste principles that typified the Greek Revival fashion then sweeping the country. Built on an elevated site blasted out of the hillside, the State House enjoyed a grand approach. On a cold night in January, 1857, a fire, caused by the wood-burning heating system, destroyed nearly everything within the granite walls. Ultimately the walls themselves would come down, leaving only the Grecian portico to be incorporated into the design of the third State House.

The third and present State House was built on the same site as the second. Its basic plan is similar to Young's, but it was built on a larger scale with a distinctly different ornamental scheme reflecting the Renaissance Revival style popular at the time. This State House was constructed over a two and a half year period, cost $150,000, and was dedicated in 1859. Additions in the rear date from 1888, 1900, and 1987.