In April 1640 Widdrington was elected Member of Parliament for Berwick in the Short Parliament. He was re-elected MP for Berwick for the Long Parliament in November 1640. As a barrister, his legal knowledge was useful during the English Civil War. In 1651 he was chosen a member of the Council of State, although he had declined to have any share in the trial of the king. He was elected MP for York in 1654 for the First Protectorate Parliament. In 1656 he was elected MP for Northumberland in the Second Protectorate Parliament and was chosen as Speaker in September 1656, and in June 1658, he was appointed Lord Chief Baron of the Exchequer. In 1659 and again in 1660, he was a member of the Council of State, and on three occasions he was one of the Commissioners of the Great Seal. He lost some of his offices when Charles II was restored. In 1660, he was elected MP for York in the Convention Parliament. He was elected MP for Berwick again in 1661 for the Cavalier Parliament.