The fourth son of Colonel Richard Tilghman and Anna Maria Lloyd, he was born at his family's estate, the Hermitage, on the Chester River in Talbot County on Maryland's Eastern Shore. After studying law, he began his practice in Annapolis and in 1743 married Anne Francis (1727–?), daughter of Tench Francis (Sr.). About 1760 Tilghman moved to Philadelphia, where he held many positions of public service, including Secretary of the Land Office of Pennsylvania (appointed by John Penn in 1765), Philadelphia City Councilman (1764), and member of the Pennsylvania Provincial Council (1767).
At the outbreak of the American Revolution, Tilghman at first favored compromise between England and the colonies; while he called for a repeal of the Intolerable Acts, which was so abhorred by colonists, he at the same time denounced the Boston Tea Party. He was regarded, however, as a Loyalist and was placed under arrest by Pennsylvania state authorities until 1778.
Tilghman was a trustee of the College of Philadelphia (now the University of Pennsylvania) from 1775 to 1788, when he resigned.
Tilghman's youngest brother was Matthew Tilghman, a delegate to the First and Second Continental Congresses. His eldest son was Tench Tilghman, aide-de-camp to George Washington during the American Revolution. His son William Tilghman became chief justice of Pennsylvania in 1806.
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