The true crime basis of the story, surrounding du Pont's attempted mentorship of two Olympic wrestlers, Mark Schultz (Channing Tatum) and his brother David (Mark Ruffalo), is weird, chilly and profoundly ambiguous.
The story is not very well known, Miller says.
"It came to me eight years ago in the form of a newspaper article someone semi-randomly gave me. I would say west of the Mississippi it's rare to encounter anyone who's heard of it and, to those who have, there's never more than a vague memory of it happening, based on pretty hasty and shallow coverage of the event - just the bare sensational facts, of the wealthiest man in America ever to be convicted of murder."
Eight years is a long time to get a film off the ground. Miller had an abortive try at it: in this first go-round, Channing Tatum was already his preferred choice to play Mark, the semi-orphaned, emotionally withdrawn freestyle wrestler who accepts an invitation to train from a reclusive aristocrat he'd never heard of.
Foxcatcher Farm is the name of the du Pont family ranch outside Philadelphia, where John established a state-of-the-art wrestling facility in the 1980s.
Why the long delay?
"Reality put it on hold," Miller says. "Circumstances forbade the film from being realised. I couldn't find the money. That's it!"
Meanwhile, he rode to the rescue on Moneyball, replacing the baseball bean counter drama's original director, Steven Soderbergh, at the behest of producer and star Brad Pitt. It was a hit for Sony, grossing $110 million worldwide. Being a project's last-minute salvation gives you the kind of brownie points in Hollywood you can't really buy. With the support of 28-year-old producer Megan Ellison - daughter of rich sports patron and former boss of Oracle, Larry - Foxcatcher got the green light.
Steve Carell, he says, might have been on the list to play du Pont early on. He gives a transformative portrait of a deeply odd, lonely and disturbed man. Miller cites Scorsese's The King of Comedy, not so much for the De Niro performance as the Jerry Lewis one.
"There was a concept of Jerry Lewis before The King of Comedy, and a concept after. The moment I saw him in that role, I was like, 'Oh, OK, he can't go back!'."
He has a ready list of other revelatory dramatic roles for comic actors - Alastair Sim in Scrooge, Peter Sellers in Lolita.
"Adam Sandler in Punch-Drunk Love is brilliant. Brilliant, brilliant.
It's not that you can't go back, but you can't put that back in the bottle. You see that there's more."
Of course, Miller directed the late Philip Seymour Hoffman to his Oscar as Truman Capote - a role that required a not dissimilar immersion inside a tricky headspace. He gave Carell Hoffman's number to ask for advice.
"I don't know if they ever spoke. Phil is not ... " He catches himself. "Was not, a mimic. He didn't do impersonations. He didn't put on characters. He was an inside-out actor. He found his way by getting Truman's voice on tape and sitting alone in a room, playing it again and again and again, working the voice, working the voice. And Steve did very similar work with a tape on du Pont that we had."
Channing Tatum shot to the top of Miller's casting list after his breakout performance in the gritty coming-of-age indie A Guide to Recognising Your Saints (2006).
"He's unbelievable in it. It was one of those moments where somebody materialises on screen and you wonder who the hell even is that. I don't know if I would have thought of Channing based on the work that followed. But all of that was essential for his maturation."
Rounding out a trio of meaty roles is Ruffalo, whose performance as David, the wary, blue-collar family man whose groundedness John comes to envy. At 47, he's significantly older than the real David was, and the physical demands of the wrestling scenes were massive.
"Age-wise, he was right on the cusp," says Miller. "He says, if this had come around even one year later, he didn't think he would have been capable. But he took it all upon himself to be physically prepared to do it, and he never made that my problem. All of these stories of the miseries required by both him and Channing never cropped up until we started doing Q&As together. They never complained to me about it. Which is very much in keeping with the culture of wrestling."
This grunting, sweaty world was completely foreign to Miller when he started research.
"It seemed like just an unseemly, bizarre sport. But I came to see it's actually an extraordinary sport, and one of the purest and one of the oldest, if not the oldest - one of the original sports of the Olympic games. It's also a sport where there's no opportunity for extrinsic reward. There's no fame or fortune available to those who succeed at the highest level in my country."
In recent weeks Mark Schultz - who served as one of the film's producers - has used social media to express his displeasure at Miller's version of events, specifically at the hints that there was a sexual undercurrent to his relationship with du Pont. Miller offers a different interpretation.
"There is an obsession with fathers and fatherliness in the film," he says, "with the founding fathers of America and George Washington, with being a patron, with being a patriot, and the irony that none of these guys ever really had a father. Just as America itself eliminated its father."
Carell's metamorphosis puts him in Oscars ring
Steve Carell's transformative performance as John du Pont and rare foray into drama has won the comedian accolades - including Golden Globe and Oscar nominations.
The 52-year-old says he is enjoying "being part of the conversation" during the awards season.
Before the film, he had little knowledge of the real-life man he portrayed, other than the television reports about the murder.
"It was a bit scary as it was unlike anything I've ever tried before. I wasn't trying to impersonate him but he had a very specific way of speaking and I tried to emulate that to provide an essence of the kind of person he seemed to be. You can only make your best guess at the type of person he was."
One of the biggest clues came from a documentary du Pont had made about himself.
"The raw footage between takes showed a different side of him. He also wrote many things." Carell spent three hours each day being fitted with prosthetics including a hooked nose.
"We took the hairline back and the eyebrows down and added different layers of skin colour because my skin tone is more Mediterranean. For months I looked in the mirror and it didn't look like me. I could also see how off-putting my presence was for the people I was working with, which was actually really good because it spoke to the relationship with du Pont himself."
- Helen Barlow
Who: Bennett Miller, director of Capote, Moneyball and now Foxcatcher, which starts Steve Carell, Channing Tatum and Mark Ruffalo.
When: Opens at cinemas on Thursday