Rutherfurd declared his candidature for Roxburghshire (where his father had been member 50 years before) in 1787, under the aegis of the 3rd Duke of Buccleuch. "His unpopularity was reported to be as positive as that of the sitting Member, Sir George Douglas, was negative, for he was 'snappish, petulant and assuming'."[9] He declined a compromise with his cousin Sir Gilbert Elliot, who ensured his defeat at the election of 1790. Soon after acquiring most of his father-in-law's fortune (who died in 1794), he assured Buccleuch in 1796 that although "his windfall enabled him to consider becoming county Member in place of Douglas, he preferred Douglas's continuing or the adoption of another candidate to coming in himself or swallowing Sir Gilbert Elliot’s return." Buccleuch accordingly considered him out of the question, but in 1802 procured his return for Selkirkshire.[9]
In December 1803, he became vice-lieutenant in Roxburghshire. After becoming the Member for Roxburghshire in 1806, he took three leaves of absence from 29 April 1812 until the dissolution.[9]
Edgerston
Since his father (who died in 1758) predeceased his grandfather (who died in 1764), upon the latter's death, sixteen year-old John succeeded to his grandfather's vast Scottish estates.[5][10] He was also heir of his uncle, Baron Robert Rutherfurd of Fairnington.[9]
Rutherfurd was known as a great benefactor to Edgerston. In 1793 he built on the two wings with their Venetian windows and the semi-circular tower at the south side of the house. In a letter written by his uncle, Baron Robert Rutherfurd to another uncle, Walter Rutherfurd, "Fairnington, Oct 28, 1788, Dear Walter, I want to send you a copy of the plan of the improvements that our nephew is making at Edgerston. He is putting on two wings at a cost of 3,000 and when it is completed it will be one of the finest seats in the Shire." In a letter between the same uncles, "Fairnington, Nov 26, 1792. Edgerston House by being repaired with additions is now one of the handsomest and most commodious of any in this county."[11]
As Rutherfurd had no children of his own, he settled the lands of Edgerston, on his nephew, William Oliver (the son of his sister Jane), who then styled himself William Oliver-Rutherfurd, who built the Tower at Edgerston in 1840.[9]