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Hamilton's first published works were short stories, "My Own Earth" and "Aunt Marj's Happy Ending", both published in Harper's Magazine in 1983. "Aunt Marj's Happy Ending" later appeared in The Best American Short Stories 1984.
Her first novel, The Book of Ruth, was published in 1988 and won the Hemingway Foundation/PEN Award, Great Lakes College Association New Writers Award, and the Wisconsin Library Association Banta Book Award in 1989. The Book of Ruth was an Oprah's Book Club selection in 1996, and it was the basis for a 2004 television film of the same title.
In 1994, she published A Map of the World, which was adapted for a film in 1999 and the same year was also an Oprah's Book Club selection. Her third novel, The Short History of a Prince, published in 1998, was a Publishers Weekly Best Book of 1998. This book was also shortlisted for the 1999 Orange Prize. In 2000, Hamilton was named a Notable Wisconsin Author by the Wisconsin Library Association.
All of her books are set, at least in part, in Wisconsin. "A Map of the World" is set in Racine County, Wis. Of her writing, novelist Laura Moriarty says: "I like Jane Hamilton for her compassionate portrayals of characters most people would ridicule, and the way her books show the beauty of rural life without romanticizing it."
In a November 2006 interview with The Journal Times, Hamilton talked about her early inspiration for writing novels. As a student at Carleton College, she overheard a professor say she would write a novel one day. Hamilton had written only two short stories for the professor's class. Overhearing the conversation gave her confidence. "It had a lot more potency, the fact that I overheard it, rather than his telling me directly," she said.
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