When a member of the Democratic Party, Cunningham narrowly defeated Republican state representative Katie Arrington in the 2018 general election.

He lost his 2020 re-election bid in another close race to Republican state representative Nancy Mace after one term in Congress.

He was the Democratic nominee in the 2022 South Carolina gubernatorial election, losing to incumbent Republican governor Henry McMaster.

Cunningham attended the College of Charleston for two years before transferring to Florida Atlantic University in 2002, where he obtained his Bachelor of Science in ocean engineering in 2005.

[6] In July 2017, Cunningham announced his candidacy for the United States House of Representatives in South Carolina's 1st congressional district.

Cunningham defeated Arrington with 50.7% of the vote, marking the first time since 1986 that South Carolina Democrats had flipped a U.S. House seat.

However, increased turnout in the heavily conservative Beaufort area undermined this trend, allowing Mace to overcome Cunningham's margin in Charleston County.

[16] On March 8, 2019, while National Oceanic and Atmospheric Administration assistant administrator for fisheries Chris Oliver was testifying at a Natural Resources Water, Oceans and Wildlife Subcommittee hearing on the effects of seismic testing on right whales, Cunningham blasted an air horn to demonstrate how disruptive commercial air guns were to whales.

[17] Cunningham stopped short of endorsing an impeachment inquiry against President Trump after the Ukraine allegations emerged, stating that a partisan rush to impeach the President would be bad for the country, but that if the allegations against Trump were true, they "represent a clear threat to the Constitution, our national security and the democratic process".

[18][19] On October 31, 2019, however, Cunningham voted in favor of a resolution to lay out rules to proceed with an impeachment inquiry of President Trump.

Cunningham was defeated by incumbent Republican governor Henry McMaster in the November election, receiving 41% of the popular vote.