Francis Fauquier pursued business and intellectual interests in London before entering colonial government. He directed the South Sea Company, served as a governor of the Foundling Hospital, and became a fellow of the Royal Society in 1753. His 1756 essay on financing the war argued for distributing its costs without placing the burden chiefly on manufacturers and laborers. In 1758 he became Virginia's lieutenant governor, administering the colony for absentee royal governors.

Arriving during the French and Indian War, Fauquier had to recruit and supply troops, protect the frontier, and negotiate financial demands with the assembly. He approved the Two Penny Act, which reduced the effective value of clerical salaries, provoking a rebuke from London. He also sought a compromise over paper currency and enforced restrictions on western land speculation. At Williamsburg his circle included William Small, George Wythe and the young Thomas Jefferson, with conversation ranging across science, politics and the arts.

The Stamp Act crisis tested his authority in 1765. He suppressed local printing of the Virginia Resolves and helped prevent violence against stamp distributor George Mercer. After Treasurer John Robinson's death in 1766 exposed major arrears, Fauquier appointed Robert Carter Nicholas treasurer, while Peyton Randolph became speaker, separating offices previously combined. Illness increasingly interrupted his work, and he died at the Governor's Palace in March 1768.