Jim Bridger respected the territorial boundaries of the Sioux and did not wish to subject emigrants to the danger of Indian attack. So he took the first train of miners and emigrants north on what was to become the Bridger Trail in the spring of 1864. Colonel Collins temporarily released Bridger from his commission as post scout at Fort Laramie on April 30. An emigrant train left Denver about May 1, and headed north to Fort Laramie bound for the Montana gold fields. Expecting a surge of emigration to Montana, Collins telegraphed his superiors on April 26 and expressed his concerns for the new route through the Powder River Basin.

"Immigration is coming rapidly; trouble with the Indians may be expected, and I need power or instructions. . . . A large party is coming from Denver to go a new route from the Platte to the mines, crossing the Big Horn and Yellowstone. . . . Other trains are coming with same object. The route will be at least 200 miles shorter, through a country that ought to be opened, but a strong military party will be necessary. . . . I have devoted the last two years to understanding this country. . . . In this mountain service it is better to lead than follow immigration. Could I have my way, it should be sifted, controlled, and guided on designated routes; not permitted to run wild and make trouble."

Bridger agreed to guide the train by the safer route west of the Bighorn Mountains and through the Bighorn Basin, which required no military escort. He left Fort Laramie on May 20 and headed west up the North Platte River for the ten-day, 140-mile trek to the Bridger Cutoff west of Red Buttes.

Jim Bridger's trail route departed the main Oregon Trail west of Red Buttes, located along the North Platte River just west of present-day Casper, Wyoming. Heading in an overall northwestern direction, the trail skirted the southern end of the Bighorn Mountains, crossed Badwater Creek, and then proceeded up Bridger Creek, passing over what today are known as the Bridger Mountains. The trail descended the northern slope of the mountains via the Kirby Creek drainage to the Bighorn River in the southern Bighorn Basin. The trail crossed to the west bank of the river near present-day Lucerne, Wyoming, and continued downstream to the north, fording the Greybull and Shoshone Rivers. The trail approached the Montana border in the vicinity of present-day Frannie, Wyoming.

Once in Montana, the trail proceeded north to Clarks Fork of the Yellowstone River, continued downstream past present-day Bridger, Montana, to the vicinity of Rock Creek where the Bozeman Trail joined Bridger's trail. From this point the two routes continued west as the Bridger Trail south of the Yellowstone River. The trail crossed the Yellowstone east of present-day Livingston, Montana. At this juncture, the respective routes of the Bridger and Bozeman Trails diverged as each guide chose a different route over the mountains in the vicinity of present-day Bozeman Pass. The routes then coalesced as a single route into the recently established community of Bozeman. The trail continued west, crossed the Gallatin River, and then proceeded to the Madison River. At that point the trail turned south up the valley of the Madison to the bustling gold mining community of Virginia City, Montana Territory.

The Bridger Trail route from Red Buttes to Virginia City was approximately 510 miles. Based on an average of 15 miles a day, with a one day layover per week, it would have taken approximately 34 days to travel the Bridger Trail route. However, time should be factored in for prospecting forays to the nearby mountain ranges along the way. After all, that was the principal reason to make the journey. Bridger's train, leading the way and taking extra time for road work, traveled the route in about 50 days. The trains that followed, some of which caught up to and passed Bridger, made the trip in as little as 34, 36 and 37 days. Howard Stanfield was with John Jacobs' train when they departed Red Buttes on May 30, ten days behind Bridger. Stanfield arrived in Virginia City 42 days later on Sunday July 10 after a trip that included many layovers, some of which were for prospecting. Cornelius Hedges left Red Buttes on June 4, and reached Virginia City on July 10; a total of 37 days including layovers. James Roberts, Robert Vaughn, and guide Joseph Knight left on June 10, and arrived on July 13. This trip of 34 days was the fastest of any Bridger Trail train. Charles Baker's train took Bridger's Cutoff on June 22 and arrived in Virginia City on July 28, for a total of 37 days on the trail. Traveling with Baker, William Atchison arrived one day earlier than Baker on July 27.