At age 10, Daniel Menaker arrived home from his progressive school in Greenwich Village with a story to tell. His teacher had asked if anyone knew the names of Columbus’s three ships, leading a girl to raise her hand and declare they were “the Atchison, Topeka and the Santa Fe.”

With encouragement from his mother, a copy editor at Fortune magazine, Mr. Menaker wrote down the account of fractured history and sent it to the New Yorker, which adapted it into a Talk of the Town item in 1951.

“I guess it set me on the road to authorial vanity and perdition,” said Mr. Menaker, who went on to write a half-dozen acerbic and poignant books and became a senior editor at the New Yorker and Random House. Along the way, he helped champion and shepherd works by authors such as Billy Collins, Alice Munro and George Saunders.

In an email interview, Saunders recalled that Mr. Menaker accepted his first story at the New Yorker and later acquired and edited his first book, “CivilWarLand in Bad Decline.”

The 1996 story collection signaled “the debut of an exciting new voice in fiction,” wrote New York Times book critic Michiko Kakutani. But by Saunders’s account, it drew little attention before Mr. Menaker wrote “a glowing letter” to the head of the American Booksellers Association on its behalf.

“It’s literally the case that Dan saved that book (and, by extension, my career),” Saunders said. “He cared that much.”

Mr. Menaker was 79 when he died Oct. 26 at his home in New Marlborough, Mass. The cause was pancreatic cancer, said his wife, Katherine Bouton. He had twice battled lung cancer, a disease that prompted him to write a memoir, “My Mistake” (2013), that examined his life and career, including his red-diaper upbringing, guilt over the death of his brother and cancer diagnosis at age 66.

“In describing his devastating diagnosis and a recurrence, he uses free-associated sentences that run as long as 115 words,” author Meryl Gordon wrote in a Times review. “It leaves the reader breathless, a deliberate choice by this onetime copy editor, who wants to rush through these excruciating episodes yet convey in lyrical fashion what he feels.”

After making his New Yorker debut as a fourth-grader, Mr. ­Menaker joined the magazine as a fact-checker in 1969 and endured a range of political and creative tensions within its hallways.

Co-workers insisted that he greet the top editor, William Shawn, with a “Hello” instead of a “Hi.” Perhaps because of his lefty upbringing, he became the only editor to sign a union card during an unsuccessful effort to organize the magazine. Film critic Pauline Kael had him replaced as her editor, apparently because he showed impatience with her practice of reading her columns aloud, with a hand cupped to her ear.

Mr. Menaker’s time at the magazine nearly ended after he quarreled over an article’s wording with Shawn, whom he described as a genius with “a martyr’s demeanor.” He was told to look for work elsewhere but never left, hanging on for more than two decades “like a shade in Hades,” as Mr. Menaker put it. He became a full editor with support from fiction editor William Maxwell, who took him under his wing.

“He was especially open to new voices, which is probably the most essential and valuable thing an editor can do,” David Remnick, the magazine’s current editor, said in a statement.

Mr. Menaker edited writers including Michael Chabon, Jennifer Egan, Mavis Gallant and a former lawyer named Elizabeth Strout, whom he called to offer encouragement after the New Yorker rejected one of her stories. “Please don’t ever stop writing,” he said.

“It would be embarrassing for me to tell you how much that meant to me,” Strout later told The Washington Post, after Mr. ­Menaker helped her get an agent and acquired her debut novel, the critically acclaimed bestseller “Amy and Isabelle” (1998), for Random House. She later earned the Pulitzer Prize for the novel “Olive Kitteridge.”

Mr. Menaker joined Random House in 1995, as new editor Tina Brown was trimming the New Yorker’s fiction pages. He retained no great affection for her or her husband, Random House chief Harold Evans, likening the couple to “the duke and the king in ‘Huckleberry Finn,’ floating down the Mississippi, affecting noble lineages, and fleecing townspeople right and left with their cons and impostures.”

Mr. Menaker remained at Random House until 2007, aside from a brief hiatus as an executive editor at HarperCollins. For four years, he led Random House’s namesake imprint as executive editor in chief.

In addition to working with authors such as Ted Conover, Deborah Garrison, Colum McCann and Salman Rushdie, he had a massive hit with the first novel he published, “Primary Colors,” a fictionalized account of Bill Clinton’s 1992 presidential campaign. The book was by political columnist Joe Klein, incognito as Anonymous. Mr. Menaker sent his edits to the author’s agent.

Tired of the publishing business, which he described as a world of “corporate foolishness and credit larceny,” he focused in recent years on his own writing, which he said he began in earnest only after the death of his older brother, Mike.

Mr. Menaker had goaded his brother during a family touch-football game in 1967, pushing him to play in the backfield despite his bad knees. He tore a ligament while trying to block a pass, then developed a fatal blood infection, septicemia, after surgery. Mr. Menaker could not forgive himself.

He turned to psychoanalysis, which featured in his only novel, “The Treatment” (1998), about a domineering Cuban analyst and a timid patient working through the early death of his mother. (It was later adapted into a 2006 movie.) Perhaps more than therapy, writing also offered a kind of solace.

“It has reaffirmed my belief that the past is the definition of inevitability,” he told the Paris Review. “I had no choice but to do what I did with my brother during the touch football game, which was to goad him slightly. He had no choice but to take up the goad and to do what he did. And so I’m kind of at peace with it.”

Robert Daniel Menaker was born in Manhattan on Sept. 17, 1941. His mother, he recalled, was merciless about grammar and proper names, once threatening to disown him for saying “Tiffany’s” instead of “Tiffany.” His father designed and sold furniture and inherited the radical beliefs of his own father, a Jewish immigrant from Eastern Europe.

In Mr. Menaker’s telling, his father traveled to Mexico in the 1930s “to keep an eye on Trotsky,” the exiled Russian revolutionary who was ultimately assassinated there. The elder Menaker was later linked to KGB intelligence operations in Chile but “seemed pretty feckless altogether,” said Mr. ­Menaker, who suspected his father was not entirely sure of what he was doing.

Mr. Menaker studied at the “aptronymic” Little Red School House in Greenwich Village, which he said “was filled with little reds,” and spent his summers living on a farm in the Berkshires owned by a communist uncle named for Friedrich Engels, who inspired many of the stories in his 1987 collection, “The Old Left.”

After graduating from high school in Nyack, N.Y., Mr. Menaker received a bachelor’s degree from Swarthmore College in 1963 and a master’s degree from Johns Hopkins University in 1965. He taught at private schools before joining the New Yorker, where he met Bouton, who was then a typist.

They married in 1980, and she later worked as a New York Times editor and wrote books on hearing loss. In addition to his wife, survivors include two children, Elizabeth and Will, a co-host of the left-wing political podcast “Chapo Trap House.”

Mr. Menaker’s later books included “The African Svelte” (2016), a collection of linguistic blunders (“The terrorist was wearing a baklava”), and “Terminalia,” a poetry collection that Portal Press is slated to publish in November.

In a phone interview, his wife said the book examined his illness and served as “a kind of therapy” for Mr. Menaker, who was diagnosed with cancer in January. He wrote in one poem: “The illness you’re fighting/ And to which you will lose was Written, like this./ But uneditable, inevitable.”