It may not have been the shot heard around the world, but five days later, it's still resounding around the vastness of the Rocky Mountains. When Robert Millage took aim just before dawn last Tuesday in the wilderness of north-central Idaho and shot dead an 80lb female wolf, he earned only a small footnote in the annals of recreation, but he reignited a controversy half as old as time.

Millage's shot from his .243 rifle, fired at about 25 yards as the animal rushed towards him, made him the first person to kill a wolf in the state's first official wolf hunt for more than three decades. And with it, a new chapter opened in the long, fraught and mostly one-sided battle between man and wolf in the American West.

In a sense, the recent history of the grey, or timber, wolf is a triumph of conservation. Once upon a time the animals roamed the continent. Then the white man arrived, and by the early 20th century the animal had been all but exterminated as the West was tamed. Barely 50,000 remained in all of North America, mostly in Canada and Alaska. Only in Minnesota did a stable grey wolf population survive south of the 49th parallel.

But wolves are no respecters of human frontiers. Protected since the early 1970s under the Endangered Species Act, a few slipped back from Canada across the rugged ranges into Montana and Idaho.

Then in late 1994 the US authorities made the immigration official by reintroducing a few dozen wolves to a swath of remote federal land in the two states. Bringing them back, however, was not easy. At the best of times the creature has an image problem, while ranchers and hunters rose against the idea, arguing that wolves would destroy livestock, as well as such traditional game as deer, elk and moose.

About that time, I made a trip to the mountains of Idaho, on what proved to be one of the most magical adventures of my life. Not that my guide or I so much as heard a wolf howl, let alone saw one. But as dusk fell they were there in spirit, somewhere out in the forest beyond the mountain pastures where owls flapped silently by and elk stood motionless in the fading light. Wolves may have had a raw deal in myth and legend, but here, unarguably, they belonged.

And not only did they belong, they flourished. By last year the wolf population of Idaho, Montana and the area around Yellowstone National Park in Wyoming was estimated to have grown to around 1,650, and in March the new Obama administration ruled that the creatures were no longer endangered.

For the first time in 35 years, wolves were once more legal game – and thus it was that Robert Millage, along with thousands of other Idahoans, paid $11.75 (£7) for a wolf-hunting tag and set out on what he called "one of the bigger occasions of my life".

In Idaho, the authorities are allowing 220 wolves to be killed, out of an estimated 850 in the state, over a season running from 1 September until 31 December at the latest, and sooner if the quota is filled more quickly. Montana has set a limit of 75, also roughly a quarter of its wolf population. Only in Wyoming is the animal still officially on the endangered list. This is not not as a result of a shortage of wolves but because the state refuses to take proper measures to protect them.

In the 15 years since wolves were reintroduced to the US Rockies, the argument has been turned on its head. When I went to Idaho in the mid-1990s, farmers and hunting enthusiasts were up in arms, claiming the return of Canis lupus would constitute a mortal threat to their livelihoods. Now it is environmentalists who are in uproar.

Why let the slaughter recommence, they say, after so much trouble has been taken to restore a viable wolf population? Groups such as Defenders of Wildlife and the Natural Resource Defense Council point out that on top of the hunting quota, wolves may also be killed if they attack livestock, so that the true threat to their numbers is much greater.

Smaller numbers in turn will make it more difficult for the three separate populations to mingle with each other and interbreed, thus increasing the risk of genetic problems. Ideally, environmentalists would like to see an overall "connected" wolf population of between 2,000 and 5,000, well above today's pre-cull level.

And they may get their way. As of Friday, a federal judge in Idaho had yet to decide whether to issue an injunction sought by wildlife supporters that would ban hunting for this season at least.

An outsider could be forgiven for wondering what all the fuss is about. We are, after all, talking about barely 1,600 animals (animals, moreover, that present no danger to humans) scattered over three states as large as the British Isles and France combined, but with fewer than three million inhabitants. Surely there's room for everyone? But that is to reckon without the passions aroused by Canis lupus – as Robert Millage has learnt to his cost.

In the course of the few days since he bagged his wolf, abusive emails and phone calls from opponents of the hunt have poured in by the hundreds. "You will burn in Hell, you piece of shit," said one email. A message on his voicemail was even more blunt: "You killer."

Millage, a 34-year-old small-town estate agent, is bemused by the unfriendly attention. A nature lover, he has hunted since boyhood. "I'm not some crazy guy out there on a four-wheeler shooting everything that moves," he told an Idaho TV station. "I'm not the one who decided we needed to have a wolf season."

The state organised the hunt, and he bought his tag. "I didn't do anything wrong so I shouldn't feel bad about it." But where wolves are concerned, nothing somehow is ever simple.