Asked by a North Carolina newspaper if the Freedom Caucus was still relevant in a Democratic-controlled House, Mr. Meadows smiled. “Oh, more relevant than you might imagine,” he said.

His role as a critical supporter of the president came as a departure for Mr. Meadows, who built a reputation on his hunger to challenge the Republican establishment and its leaders. In an escalation of the bad blood simmering between the right flank of the Republican conference represented by Mr. Meadows and the more centrist leadership, in 2015 Mr. Meadows attempted to overthrow Mr. Boehner, ultimately influencing the then-House speaker’s decision to retire early.

Under Mr. Ryan’s tenure as speaker, the House Freedom Caucus, led by Mr. Meadows, continued to flex its muscles as the most powerful group of lawmakers in Congress.

While praising his conservative record, Republican lawmakers also underscored another, more unusual aspect of Mr. Meadows’ congressional career: his ability to build friendships across the aisle.

“Not only is Mark a top-notch conservative, he’s an upstanding individual, who looks to build friendships with all of his colleagues,” Representative Andy Biggs of Arizona, the current chairman of the Freedom Caucus, said in a statement. “In a growing partisan climate, Mark’s example is a breath of fresh air and one that we all should strive to emulate.”

In one of the more improbable alliances in Congress, Mr. Meadows counted as a close friend the late Representative Elijah E. Cummings of Maryland, who served as the chairman of the powerful Oversight Committee. The two worked together on prescription drug legislation, and when Mr. Cummings died in October, Mr. Meadows delivered an emotional eulogy.

As Mr. Meadows eyes his next job, it is not immediately clear who his successor might be. Friday is the deadline to file for re-election in his heavily Republican congressional district — a short turnaround time for any potential candidate.