As the new nation began after the passage of the Constitution, the political structure quickly began to fragment along ideological lines. Monroe fell into what came to be known as the Anti-Federalist party. He largely opposed the strong, centralized federal government forwarded by people like Alexander Hamilton, the head of the Federalist party. Thus, when Virginia formed its congressional districts, it raised more than a few eyebrows when the district that included the home county of James Madison–one of the leading federalists–also included the home of James Monroe. Monroe did not want to run against his old friend Madison, but he felt that public service was a duty and so, if requested to run, he could hardly turn down the position. Madison, for his part, understood this and never held it against Monroe. In the end it barely mattered, for Madison won handily; within a few days of the election, the correspondence of the two men began anew.

In the spring of 1790, Monroe lost another race–one that he didn't even know he was in. The Governor's Council had voted to appoint an interim senator and Monroe lost by a single vote. Thomas Jefferson and other anti-federalists were not pleased with the vote and later urged Monroe to run in his own right in the fall elections. Even without the support of Patrick Henry, perhaps the dean of Virginia's anti-federalists, Monroe won the senate race easily. In December 1790, he was seated in the Senate, in Philadelphia, which would remain the seat of government for another decade.

Monroe threw himself into the work of the Senate; in the first session of the body, he and ten others held nearly every important committee assignment and even chaired a committee considering a proposal by Virginia to grant pensions and bounties to men who served in the Revolution. During this time, the Senate was much lower-key than the House, where the true political battles raged, battles like the Bank of the United States. In general, Monroe supported states' rights and opposed the foreign policy of President George Washington–policies that Monroe felt were too easy on the British. He opposed the appointment of Gouverneur Morris as Minister to France and although Morris was eventually confirmed, the tight confirmation made Washington realize the power Monroe wielded. On several future appointments, Washington cleared them with Monroe first.

In between legislative sessions, Monroe journeyed home to Virginia and worked at his law office in Fredericksburg. Their two children kept Monroe and his wife Elizabeth busy, and Monroe also made numerous trips around the state meeting with other politicians. He was a star on the rise.

Over the course of the spring and summer of 1793, Monroe's life would take a decidedly new twist. To Monroe, Washington's foreign policy had taken a serious turn–his proclamation of neutrality appeared to be an end move towards an anti-French policy. The growing troubles between Britain and France threatened to draw the weak America into a war it was ill-equipped to fight. Nevertheless, Monroe condemned the policy, one to which he had not originally objected, as an unconstitutional attempt to prevent Congress from declaring war. However, no one could clearly articulate the nation's stance towards France. Finally, word leaked out that the minister from France himself was planning to equip a privateer in violation of Washington's orders. When the privateer sailed, in direct violation of Washington's decision, Washington asked for the minister to be recalled. Monroe, who favored friendly relations with France, found himself thrust into the middle and his efforts and that of other Anti-Federalists helped ensure more favorable treatment.

Monroe showed a key political nature during his time in the Senate. When the Federalists successfully ejected Albert Gallatin, an anti-federalist from Pennsylvania, because Gallatin had not been a U.S. citizen for the required nine years, Monroe led the fight in support of the Pennsylvania senator–only to lose by a vote of fourteen to 12. Monroe brooded quietly and waited several months for revenge. When Kensey Johns, a Federalist from Delaware, arrived to be seated in the body, Monroe rose and objected that since the state legislature had convened a session in between Johns's appointment by the governor and Johns's arrival in Philadelphia, the governor had no right to make such an interim appointment. The matter was referred to a committee that determined Monroe was right–Johns could not be seated.

Towards the end of 1793, Monroe again found himself swept up in the American- French affairs. Gouverneur Morris had been recalled, and Washington now looked to appoint a new minister. After a brief flirtation with several other candidates, Washington settled on Monroe as the new emissary. Ironically, after leading so many controversial fights over presidential appointments, Monroe's appointment sailed through the Senate with hardly an ill-word. Within a fortnight, Monroe rode for Baltimore to sail to France. The relations between the two countries were much too fragile to take time to return to Virginia and settle his affairs.

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