In 1866 and again in 1869, Carlisle was elected to the state senate, where he spoke out against Radical Reconstruction.  In 1871, he was elected Kentucky’s lieutenant governor, allowing him to gain parliamentary experience while presiding over the state senate.  In 1876, Carlisle won election to the first of seven consecutive terms in the U.S. House of Representatives (1876-1890).  He lobbied unsuccessfully for the repeal of the Specie Resumption Act of 1875, which returned the U.S. to the gold standard in January 1879.  He took a moderate bimetallist position, endorsing the use of silver as well as gold, but opposing the inflationist policy of the unlimited coinage of silver (free silver).  When the Democrats won control of the House in 1878, Carlisle’s outspoken support of the Democratic attempt to roll back the civil rights legislation of Reconstruction earned him respect among his partisan colleagues, although Republican president Rutherford B. Hayes vetoed the bills.

As a member of the powerful House Ways and Means Committee, Carlisle pushed for tariff reduction, arguing that high tariffs helped only special business interests to the detriment of farmers, workers, and consumers.  During the acrimonious debate in Congress, which resulted in passage of the Mongrel Tariff of 1883 (so named because it was a compromise which did not satisfy either side), Carlisle emerged as a leader of the low-tariff/free trade Democrats.  In December 1883, he won the House speakership over trade-protectionist and former speaker Samuel J. Randall of Pennsylvania, and was reelected in 1885 and 1887.  Following the Democratic loss of the House in 1888, Carlisle served as minority leader, and vigorously opposed the new rules imposed by the Republican speaker of the house, Thomas B. Reed of Maine, which enhanced the speaker’s authority.  The timing of Carlisle’s election to the U.S. Senate in May 1890 to fill a vacated seat, allowed him to vote against the protectionist McKinley Tariff in both houses (the bill passed both). 

When Cleveland was reelected president in 1892, he appointed Carlisle as treasury secretary.  The slowing economy of 1892, under the watch of President Benjamin Harrison, grew into a full-fledged depression shortly after the Cleveland administration took office.  Carlisle and Cleveland lobbied for Congress to repeal the Sherman Silver Purchase Act of 1890 during a special session in 1893.  It passed, but the debate further divided the hard money (gold standard) and soft money (free silver) wings of the Democratic Party.  The Treasury Department’s sale of bonds to J. P. Morgan’s banking syndicate provoked heated criticism.  When the Democrats nominated free-silver champion William Jennings Bryan of Nebraska for president in 1896, Carlisle backed the ticket of the breakaway Gold Democrats.  At the close of the second Cleveland administration in March 1897, Carlisle largely retired from public life and practiced law in New York City, where he died on July 31, 1910.