Ms. Fleming, a Sag Harbor attorney who ran on the Democratic and Independence lines, won 3,203 votes. Mr. Hughes, a retired Southampton Town Police lieutenant from Hampton Bays who ran on the Republican line, received 2,662.
Even with Ms. Fleming's victory, three Republicans will hold the majority on the five-member board. They are council members Chris Nuzzi, Jim Malone and Nancy Graboski.
Less than 16 percent of registered voters in the town cast a ballot in Tuesday's election.
It was held to fill a vacancy created on the Town Board after former Town Board member Anna Throne-Holst was sworn in as town supervisor in January. Ms. Throne-Holst, running on the Democratic. Independence and Working Families lines, beat the incumbent, Republican Linda Kabot, in the November election.
It was Ms. Fleming's second bid for a Town Board seat within half a year. She ran unsuccessfully for Town Board in November.
Ms. Fleming said she was thrilled Wednesday morning in a phone interview. She pulled over to talk, she said, saying that she was driving around Southampton Town taking down her campaign signs.
"I am gratified and honored by all the support," she said. "Now it's time to get to work."
She said her first order of business would be voting in favor of a resolution to hire a Southampton Town sustainability coordinator and a resolution for road paving.
A swear-in date has not yet been set, though Ms. Fleming said it could be as early as March 16. Her term will expire when Ms. Throne-Holst's would have, Dec. 31, 2011.
Ms. Fleming is a former assistant district attorney in Manhattan, where she was chief of the DA's welfare fraud unit. She and her husband, Bob, who is a carpenter, moved to the Sag Harbor area of Southampton Town about 10 years ago and have a son.