In 1862, President Lincoln named Davis to the United States Supreme Court, where he would serve for fourteen years.  His most important majority opinion on the nation's high court was in Ex parte Milligan (1866).  The case involved a civilian who had been tried and found guilty by a military court in Indiana for aiding the Confederacy during the Civil War.  The Supreme Court ruled that civilians could not be tried by military courts in areas that were not theaters of war and where the civilian courts were operating, thus overturning Milligan's conviction.  Davis voted with the majority in Georgia v. Stanton (1867) to uphold the Congressional program of military-enforced Reconstruction in the post-war South.  He also joined the majority to approve the federal government's authority to print paper currency in the Legal Tender Cases (1870-1871) and to sanction state government regulation of business in Munn v. Illinois (1876).

Davis had worked for Lincoln's reelection in 1864, but was dismayed by the president's Emancipation Proclamation.  Although the justice supported the constitutionality of Reconstruction, he disapproved of the Radical Republicans' implementation of it, and finally broke with the party when it impeached President Andrew Johnson.  By the early 1870s, Davis had become bored with life on the bench and yearned for elective office.  In early 1872, he was nominated for president by the tiny Labor Reform Party and was a front-runner for the nomination by the breakaway Liberal Republicans until his candidacy was derailed by a group of Liberal Republican newspaper editors. 

In early 1877, Congress passed the Electoral Commission Act to resolve the disputed Electoral College returns of the 1876 presidential election.  It was assumed that Davis would be the fifth justice and the only independent on the 15-member commission that was otherwise evenly divided between Republicans and Democrats.  Instead, on January 25, a Democratic-Greenback coalition in the Illinois legislature elected Davis to the U.S. Senate, and he promptly resigned from the commission.  The substitute fifth justice, Joseph Bradley, was a Republican who cast his every vote to ensure the election of Republican Rutherford B. Hayes.

In the last two years of Davis's term, the U.S. Senate was evenly divided with 37 Republicans, 37 Democrats, and two independents.  In March 1881, Davis announced that he would vote on organizational matters with the Democrats but would remained independent of party affiliation on substantive issues.  When William Mahone, a Virginia Democrat turned independent, decided to vote with the Republicans, his vote plus that of Vice President Chester Arthur gave the Republicans temporary control of the Senate.  After Congress reconvened in October 1881 following the death of President James Garfield, Davis was elected president pro tempore of the Senate.  In the absence of a vice president, he was next in line for the presidency.

Davis did not seek a second term in the Senate, but retired in 1883 to Bloomington, Illinois, where he died three years later.

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