He spent 10 years (1824–34) in the United States House of Representatives as a National Republican (later Whig), where he supported protectionist tariff legislation.

His second term as governor was undistinguished, but he split with fellow Whig Daniel Webster over a variety of issues, and lost the 1843 election to Democrat Marcus Morton.

He opposed the Mexican–American War, and worked to prevent the extension of slavery to the territories, although he did not take a hard line on the matter, voting for most of the provisions of the Compromise of 1850.

His political support came from textile interests and a faction of the National Republicans (later Whigs) led by Abbott Lawrence, as well as outgoing Governor Levi Lincoln Jr.[6] In the election Davis gained a plurality of votes, but not the majority that was then required.

[7] The Whig-controlled legislature did nothing to reward the Anti-Masons for Adams's move, breaking up any chance that the two parties would form a working relationship.

Davis was reelected in 1834, aided by a general dislike in Massachusetts for President Jackson's attacks on the Second Bank of the United States.

(Adams's son Charles Francis believed that Webster and Everett conspired to achieve this end, but there is no evidentiary support for the idea.

This dispute with the United Kingdom concerned the boundary between Maine and the British (now Canadian) province of New Brunswick, and had only been partially resolved after the 1794 Jay Treaty.

Massachusetts, which Maine had been a part of prior to 1820, maintained a property interest in some of the disputed land;[12] Davis took a hard line on the matter, insisting that the United States should not surrender any of the territory it claimed.

[6] In 1836 Davis sat on a special committee formed to consider legislative responses to a flood of allegedly inflammatory abolitionist materials being sent into southern slave states from northern anti-slavery organizations.

When John C. Calhoun introduced legislation criminalizing the mailing of such materials, Davis spoke out against it, pointing out that it would effectively act as an unconstitutional gag on people seeking to speak out against slavery.

[19][20] Not long after Marcus Morton won the 1839 gubernatorial election, Whig leadership prevailed on Davis to run again for governor.

This period in office, like his first term as governor, also did not contain any new programs or initiatives, but was overshadowed by the ongoing negotiations between Daniel Webster (now Secretary of State) and Lord Ashburton over the boundary issue.

[6] In 1842 the anti-slavery Liberty Party had risen to sufficient prominence in the state that neither Morton nor Davis was able to secure a majority.

[27] Davis was opposed to slavery and its extension into the territories, but he voted for most of the provisions of the Compromise of 1850,[28] including the bill on Texas borders, shocking some anti-compromise Whigs.

[29] He regularly voted in favor of the Wilmot Proviso, a measure to ban slavery from territories won in the Mexican war which was frequently attached to legislation in the late 1840s but was never adopted.

[31] Davis's weak stance on slavery began to cause a decrease in his popularity as abolitionist sentiment in the state gained ground during the 1840s.