In the spring of 1830, Congress passed a bill authorizing widespread internal improvements. Although President Jackson quietly vetoed it, Congress soon appeared to be moving toward over-riding the veto. Polk, a long-time opponent of internal improvements, almost single-handedly blocked the override. He campaigned tirelessly, rallying other supporters of states' rights to his cause and voicing the dangers of the move to state sovereignty. When the override motion failed, it cemented Polk's position as one of Jackson's main fighters in the House. Thus, it did not surprise Polk when Jackson asked him to head up the Congressional fight against the so-called "hydra-headed monster," the Second Bank of the United States.

Jackson saw the national bank as a misuse of government funds and a dangerous financial apparatus just waiting to cause another financial panic like the one it had caused in 1819. Nicholas Biddle, the head of the bank and a sworn enemy of Jackson, had managed to convince many congressmen (partially through illegal loans and preferential treatment) that the bank needed to be rechartered–partly proving Jackson's point that the bank could wield enormous influence over the government. Jackson knew that the bank did stabilize the country's financial system, so he set about establishing a new depository within the treasury department where the government could deposit its money. When the issue came before the House in 1832, Polk cited twenty-one instances where the bank had violated its charters and he asked that a special committee be appointed to investigate. Despite an unfavorable recommendation from the committee, the House concurred with the Senate in granting a twenty-year extension of the charter and the bill passed to the president who summarily vetoed it.

After the election of 1832, during which Jackson defeated the bank's main supporter, Henry Clay, by a margin of more than four-to-one, Jackson returned to office invigorated for the coming fight. He had Polk promoted to the House Ways and Means committee. Polk summoned the bank's directors to testify in front of the committee where they admitted widespread fraud and corruption. Again, the majority of the committee sided against Polk–despite the revelations–and Polk and two other congressmen issued a minority report condemning the bank. Biddle's supporters tried valiantly to defeat Polk's bid for reelection in 1833, but after Polk, like Jackson, won overwhelmingly he returned to Washington ready to finish off the bank.

Polk rose to the chairmanship of the Ways and Means Committee in the new Congress. And as the president tried to force the secretary of the treasury to withdraw the government's funds from the bank, Polk rose to the president's defense again in Congress. Polk's carefully crafted and logical speech on December 13, laying out the abuses and corruption of the bank and its negative influence on American fiscal policy, marked a turning point in the battle. At the end of April 1834, Polk succeeded in passing his committee's report condemning the bank and its managers. A month later, he successfully tabled resolutions in the Senate in support of the Bank.

Just a few days after the end of the long Bank wars, the Speaker of the House suddenly resigned. Polk found himself running for the post against John Bell, another Tennessee congressman. Although early ballots saw Polk in the lead, Bell won the majority on the tenth ballot. The race prefaced a growing disconnect in the Democratic Party and a split between Bell and Jackson.

Jackson had made it clear that he hoped to position Martin Van Buren for the presidency in 1836, but now a movement arose to run Tennessee Senator Hugh Lawson White for the Democratic ticket. Davy Crockett joined with Bell to split the Tennessee party, and although Jackson could not believe his friends would turn against him, he prepared to fight for his man and to preserve his legacy.

Meanwhile, back in Tennessee, Polk had decided to sell his plantation and to try for a bigger profit in Mississippi. On September 26, 1833, Polk had written his wife that he had sold the property for six thousand dollars. He and a partner then formulated plans to open a new plantation on un-cleared land in Yallobusha County, Mississippi. When Polk's partner asked him to procure more slaves for the new land, Polk found them hard to come by. The entire nation was expanding rapidly, and the end of the Second Bank of the United States–and the subsequent redistribution of millions of government dollars into private banks–had helped fuel a massive building spree. The railroads were beginning to expand rapidly and many people had turned their eyes westward to the vast open lands that stretched to the Pacific coast. As Polk headed home in 1835 to run for reelection, he knew that both his career and America stood on the verge of something new and exciting.