The two candidates were pitted against each other, as was the country, each holding opposite viewpoints on the expansion of slavery and popular sovereignty. Lincoln's position was that the Union was at risk and needed unified action. Although he was against the creation of new slave states, he sought to placate the southern public by saying that slavery should not be removed from those territories where it already existed (although the majority of southerners did not believe that he meant this). Douglas believed that states should have a right to choose whether to be a slave or free state. He had previously enjoyed a strong following of southern proslavery supporters, but upset many of them by supporting the Republicans refusal to admit Kansas to the Union as a slave territory.

The interwoven issues of states' rights and the expansion of slavery culminated in a question crafted by Lincoln that made Douglas address a contradiction: how a territory could in fact have popular sovereignty in view of the Dred Scott Decision, which effectively made slavery legal in all territories? Douglas's reply, that a territory could be a free territory by not establishing local slaves codes, enraged his southern proslavery supporters and became known as the Freeport Doctrine.

The decision on slavery in individual states and territories had been revisited in a series of legislative reversals that began with the Missouri Compromise (1820-21), which admitted Missouri into the Union as a slave state, while prohibiting slavery in the areas of the Louisiana Purchase. The Compromise of 1850 enacted a number of resolutions that included popular sovereignty in some areas and free states in others, and also enlisted federal support for fugitive slave laws. The Kansas-Nebraska Act (1854) granted US territories the right to decide for themselves whether or not to permit slavery, and was followed by the Dred Scott Decision (1857), which effectively made slavery legal in all territories.

Soon after Lincoln accepted the Republican nomination to run for Senate in his famous ‘House Divided’ speech, proclaiming, ‘A house divided against itself cannot stand’, he challenged the incumbent Douglas to a series of debates. Douglas, already well known for his integral role in the Kansas-Nebraska Act, which had lost him some Democratic support yet gained some Republican, readily accepted. In one particular debate Douglas retorted that, ‘this republic can forever exist divided into free and slave states’. Each of the debates lasted three hours; the first candidate stated his case in the initial hour, the second spoke for an hour and a half, and the first speaker would reply in the last half hour of the debate. Spectators numbered from 6,000 to 15,000 on each occasion.

Although Douglas won the election and served as senator of Illinois that term, the Freeport Doctrine eventually led to the split of the Democratic Party and his loss of the future presidential campaign to Lincoln, who had gained national recognition from the debates.