In 1834 Lincoln's decision to run for the state legislature for a second time was strongly influenced by his need to satisfy his debts, what he jokingly referred to as his "national debt", and the additional income that would come from a legislative salary. By this time Lincoln was a member of the Whig party. His campaign strategy excluded a discussion of the national issues and concentrated on traveling throughout the district and greeting voters. The district's leading Whig candidate was Springfield attorney John Todd Stuart, whom Lincoln knew from his militia service during the Black Hawk War. Local Democrats, who feared Stuart more than Lincoln, offered to withdraw two of their candidates from the field of thirteen, where only the top four vote-getters would be elected, to support Lincoln. Stuart, who was confident of his own victory, told Lincoln to go ahead and accept the Democrats' endorsement. On August 4 Lincoln polled 1,376 votes, the second highest number of votes in the race, and won one of the four seats in the election, as did Stuart. Lincoln was reelected to the state legislature in 1836, 1838, and 1840.

When Lincoln announced his bid for reelection in June 1836, he addressed the controversial issue of expanded suffrage. Democrats advocated universal suffrage for white males residing in the state for at least six months. They hoped to bring Irish immigrants, who were attracted to the state because of its canal projects, onto the voting rolls as Democrats. Lincoln supported the traditional Whig position that voting should be limited to property owners.

Lincoln was reelected on August 1, 1836, as the top vote getter in the Sangamon delegation. This delegation of two senators and seven representatives was nicknamed the "Long Nine" because all of them were above average height. Despite being the second youngest of the group, Lincoln was viewed as the group's leader and the floor leader of the Whig minority. The Long Nine's primary agenda was the relocation of the state capital from Vandalia to Springfield and a vigorous program of internal improvements for the state. Lincoln's influence within the legislature and within his party continued to grow with his reelection for two subsequent terms in 1838 and 1840. By the 1838–1839 legislative session, Lincoln served on at least fourteen committees and worked behind the scenes to manage the program of the Whig minority.