Challenging District 15Democratic representatives Margarette Leach, Kevin Craig, and Jim Morgan, Miller placed in the four-way three-selectee 2004 Republican primary, but lost the six-way three-position general election on November 2, 2004. Challenging the incumbents again, Miller placed in the six-way three-selectee 2006 Republican primary and was elected in the six-way three-position general election on November 7, 2006, unseating Leach. Incumbent Democratic representatives Craig and Morgan were re-elected. Miller placed first in the three-way Republican primary on May 13, 2008, with 2,116 votes. She then placed third in the six-way three-position general election on November 4, 2008, with 8,163 votes, behind incumbent representatives Craig and Morgan and ahead of non-selectee candidates Democrat Carl Eastham, and Republicans James Carden and Paula Stewart. Miller placed first in the three-way Republican primary on May 11, 2010, with 1,505 votes. She then placed second in the six-way three-position general election on November 2, 2010, with 6,601 votes, behind incumbent representative Craig and ahead of Morgan and non-selectee candidates Democrat Matthew Woelfel, and Republicans Patrick Lucas and Douglas Franklin. With all three incumbent District 15 representatives redistricted to District 16, Miller placed first in the Republican primary on May 8, 2012, with 1,745 votes,. She then placed second in the five-way three-position general election on November 6, 2012, with 8,415 votes, behind incumbent Democratic representative Craig and ahead of incumbent Democratic representative Morgan and non-selectee candidates Democrat Sean Hornbuckle and Republican Mike Davis.
On May 8, 2017, incumbent U.S. Representative Evan Jenkins announced his intention to run against incumbent Democratic U.S. Senator Joe Manchin. In August 2017, Miller announced her intention to run to fill Jenkins's seat. On May 8, 2018, Miller defeated State Delegate Rupie Phillips and State Delegate Marty Gearheart. Miller received 23.8% of the vote, and only won three of the 18 counties in the district. Miller went on to face State Senator Richard Ojeda. Many polling outlets considered this race to be a Lean Republican or a tossup. However, on November 6, 2018, Miller defeated Ojeda, receiving 56.4% of the vote. Miller won all but two counties in the district. Upon election, Miller became the first woman to represent West Virginia's 3rd congressional district and the only Republican woman to be elected to an open seat in 2018.