The logjam finally broke in July 1909 when suddenly not one but two railroads started building parallel lines down the Deshutes River canyon from the mouth of the Columbia River. The two railroads were the Oregon Trunk (OT), which was controlled by railroad magnate James J. Hill, and the Des Chutes Railway, which was controlled by competing railroad magnate Edward Henry Harriman's Union Pacific (UP). Excitement in central Oregon grew as the construction on these two line progressed. However, Prineville's excitement quickly turned to bitter disappointment as the two railroads bypassed Prineville in favor of the new town of Bend, which was located on the Deschutes River 35 miles southwest of the city. The two competing railroads eventually inked a deal that saw the two companies use one route combined from the best portions of the two partially completed routes. James J. Hill drove the final spike completing the railroad into central Oregon at Bend on 5 October 1911.

Prineville had been snubbed. The city felt helpless, and almost as soon as the railroad to Bend was finished businesses started moving from Prineville to the town that had a railroad. The usual fate of any established community left off the line of a railroad at the time was at best a quick death and at worst a long, slow decline. Bend quickly captured most of the trade business that Prineville depended on, and then other communities located along the railroad started siphoning off what was left. Prineville needed a railroad to stay alive, and the citizens initially pegged their hopes on a branchline to be built by one or both of the railroads operating to Bend. However, neither of the big roads showed any interest in building such a branchline. The townspeople gradually came to realize that if the town was to survive it needed a railroad, and if no one else was going to build a railroad to them then they would have to build one themselves.

Local concerns started thinking about building a railroad out of the city around 1909. Various groups of citizens formed two companies, the Prineville & Eastern in 1911 and the Metolius, Prineville & Eastern in 1912. The MP&E actually raised money and secured a right-of-way, but the company collapsed in 1914. There were a couple additional plans and attempts, but nothing came of any of them. It became increasingly clear that private investment in a railroad to Prineville was not easily forthcoming.

If private investment did not work, then public investment might, and that avenue became the last possible hope for construction of railroad to Prineville. The city council discussed the idea and examined the results of other such municipally built shortline railroads around the nation. On 3 March 1916 the council passed Ordinance #231, which authorized the city to build a railroad line, to sell or lease it to private enterprise upon completion, to issue $100,000 in bonds to finance construction, and to levy taxes to cover bond obligations. The ordinance went to the voters in a special election held on 28 March 1916. The ordinance passed by a vote of 355 to 1. The city council confirmed the bonds issue on 2 May and called for bids for the bonds. However, no bids were forthcoming, and the first attempt failed. On 7 July 1916 the council passed Ordinance 234, which authorized the same thing as Ordinance 231, but contained some provisions to make the bonds more appealing. This ordinance also went to the voters, who approved it by a vote of 358 to 1. A buyer was found for the second set of bonds, and the city council finalized the action on 20 January 1917.

City engineer H. A. Kelley, W. E. Burkhalter of the Spokane, Portland & Seattle Railroad, and H. J. Roberts of the Oregon-Washington Railway & Navigation Company selected the route of the new railroad. The selected route crossed the Crooked River just west of Prineville and then followed the river for a dozen miles to the crossroads known as O'Neil. From O'Neil the railroad climbed a 2.5 percent grade to get out of the canyon. Once out of the canyon the railroad made a short flat run to a connection with the joint Oregon Trunk/Union Pacific line about halfway between Redmond and Terrebonne at a point that became known at Prineville Junction. The city council authorized its attorney to obtain right-of-ways in October 1916. The city council asked landowners to donate right-of-ways with a great deal of success, with right-of-ways condemned across lands owned by those who would not donate to the cause. Grading the line came next, and E. T. Johnson and Son, a Portland-based contractor, beat out four other bidders. Grading started on 2 April 1917 in Prineville, with the grade completed in December. The city opted to lay rails with its own forces, but the company quickly ran into trouble obtaining the needed materials. By this point World War I was in full swing, and any rail purchases had to be approved by the U.S. Government. The city obtained approval to obtain the needed rails only after one of Oregon's Senators intervened. The Oregon Trunk and Union Pacific companies agreed to lease rails to the city. City construction crews laid the first rails at Prineville Junction on 30 May 1918, and the line was completed in early August. The next month was spent dumping ballast and doing other work needed to get the new property ready for operation, and the first revenue movements rolled over the new railroad in mid-August, regular freight service was established by early September, and regular passenger service was established by the following April. Increased prices on everything caused by the on-going war meant that the city was paying far more for everything that what it had planned, with the result that the city had to approve two more bond issues to secure the needed money. The voters passed the first bond in September 1918 by a vote of 127-9 and the second bond in March 1920. The city spent a total of $325,000 building the line. Prineville finally had its railroad.

The city council set up a railroad commission on 6 August 1918 and turned operations over to the new entity on 21 April 1919. The city intended to sell the railroad to private owners once the line was built, but the only investor who expressed interest in purchasing the line from the city elected not to pursue the deal. The city resigned itself to operating the railroad it had built. To start operations the new railroad purchased a new gasoline powered railbus from the White Company, a used steam locomotive, and a used passenger coach. The initial schedule implemented on 13 April 1919 saw four trains a day each way across the railroad, with two of the round trips made with a mixed train and the other two round trips made with the railbus. However, traffic did not live up to expectations, and the frequency of service gradually decreased. Early freight traffic was about two thirds seasonal livestock movements, with a number of different commodities (mostly inbound merchandise) making up the rest.

The city built the railroad with the expectation that the line would be able to pay its own way. Initial financial reports indicated that the line might be able to do that, but after a year or two of profitable operations the sudden influx of cars and improved roads caused the bottom to fall out of the passenger business, which provided the bulk of the revenue in the early years. The railroad started losing money by the early 1920s, forcing the city to advance money to the railroad. The railroad was in quite a financial hole by the mid-1920s, but was able to nearly climb out of that hole when the Depression hit. In May 1931 the city council started budgeting monthly amounts to cover the mounting deficits incurred by the railroad. Further efforts to sell or lease the railroad to private interests yielded some discussions but no deals, and the city maintained ownership and operation of the railroad. One of the biggest financial obligations faced by the railroad and the city was interest on the construction era bonds, and in 1938 the city refunded the bonds at a much lower interest rate to reduce the crushing burden of meeting the interest payments. Through this entire period railroad expenses were kept at absolute minimums, with all maintenance expenses limited to what was absolutely necessary to keep the railroad going. The city did briefly experiment with an ordinance levying a tax on all freight shipments to and from Prineville shipped via means other than the City of Prineville Railroad, but the tax did more harm than good and was quickly repealed.

The city put up with the railroad and its losses for one reason. The Ochoco Mountains east of the city were covered with a thick blanket of fine forests, mostly owned by the U.S. Forest Service. The city knew that sooner or later those forests would be opened to harvesting and that sawmills would be needed to turn logs into lumber. Prineville was the ideal place to locate such sawmills, but without a railroad the mills and their attendant jobs would bypass the town in favor of locations along the mainline railroads to the east. The first lumber mill to ship finished products went into operation in 1925. Sawmill operations gradually expanded. New larger mills came on line in 1938, and by 1940 four large mills were up and running. However, by this point the deferred maintenance of the previous decade and a half meant that the line was in terrible condition. Ties and rail were bad, ballast was non-existent, and the equipment and rolling stock was in poor shape. The railroad borrowed $28,000 from the two connecting mainline roads in 1938 to do work on the worst spots. The mainline roads also built a new $30,000 scale in Prineville so that the shortline could deliver cars to them already weighed. The railroad earned a small profit in 1939, its first since 1920. 1939 also saw the end of passenger operations.

World War Two had little impact on the railroad's traffic levels, which remained at record levels. However, shortages of men and materials forced the railroad to neglect its property, and by the end of the war the tracks and equipment were once again in poor shape. Derailments became common, and the city started receiving immense pressure from the lumber companies and regulatory agencies to fix the tracks. Finally in 1945 the city was in a position to start the re-building and re-equipping of the entire railroad. The entire railroad was re-built, the old and frail bridge across the Crooked River was replaced, and serviceable locomotives were purchased to replace the older, worn out power. The livestock business, long a staple of the company, finally disappeared in the early 1950s, but the lumber and forest products business remained strong. Profits on the railroad became a normal event, eventually allowing for the repayment of the last of the construction era bonds in 1960. Profits from the railroad allowed the city to remove all property taxes for a while in the 1960s and 1970s.

The railroad purchased its first diesel locomotive in 1950, and it scrapped the last steam locomotive on the property in 1955. Operations during the early to mid-1950s saw two round trips a day to Prineville Junction, one during the day and one at night. A decrease in lumber loads allowed the railroad to run only one train a day starting around 1960, but by the late 1970s the company was back to running two trains a day over the railroad. Traffic through this period was almost all lumber and woodchips, with occassional inbound loads of tires bound for tire giant Les Schwab. Lumber moved both inbound and outbound over the railroad, as there were a number of millwork facilities in Prineville that received rough cut lumber for futher milling. In 1978 the railroad served nine lumber related facilities in Prineville. The railroad did make one foray back into the passenger business in 1964 when the railroad purchased a streamlined coach from the Union Pacific for $5,400. The coach was used to handle special charters by civic groups and others. This coach lasted into the mid-1970s, when it was retired and scrapped. The City of Prineville Railroad also entered the incentive per diem boxcar craze of the late 1970s with the lease of 400 modern 50-foot double door boxcars from Itel in 1977. These boxcars were painted orange and featured a large map of the state of Oregon with the location of Prineville marked on the map.

The bottom fell out of the freight business in 2001. The two remaining sawmills on the line at the time were operated by the Ochoco Lumber Company and Crown Pacific. The first of the two to go was the Ochoco Lumber Company, which closed for good on 1 August. Ochoco Lumber Company was good for 800 loads a year, and its loss hurt the railroad significantly. The other shoe dropped on 22 August when Crown Pacific announced that they would be closing their Prineville mill within 60 days. Crown Pacific closed its doors and shipped its last loads in October of 2001. Traffic on the railroad dropped from 2,500 loads a year to less than 100, almost entirely inbound lumber destined for Woodgrain Millworks. By this point the railroad had a $5 million emergency reserve fund built up. The railroad elected to live off that while it searched for new revenue.

Financial results on the railroad through the next several years were dismal. The railroad lost $305,000 in 2002, $572,000 in 2003, and around $100,000 in 2004. The only real bright spot for the railroad during this time came in late 2002 when the railroad handled many loads of inbound logs. The logs had been harvested in the burned areas of a couple Arizona Indian reservations during that summer, and the affected tribes elected to salvage the burned timber and sell it to various sawmills up and down the west coast. The vast majority of this burned timber was sold to Sierra Pacific Industries, who shipped the logs by rail to their sawmills in Susanville, Chinese Camp, and Standard, CA. The logs handled by the City of Prineville were reloaded onto trucks in Prineville for delivery to a small sawmill in Prairie City, OR. This movement was a one time event, and once the last of the logs arrived the traffic was gone. Expenses were again cut to the bare bones. The railroad's management considered many options to make the railroad profitable again, and by late 2003 things began to fall in place. The first positive came when the railroad opened a new transloading facility in an abandoned sawmill complex. The facility quickly landed its first steady customer, the Louisiana Pacific laminates plant in Hines, OR, which started receiving six or seven loads of veneer and shipping out four loads of laminated beams each week. L-P used trucks to transport their products between Hines and Prineville. The next moves came during the closing months of 2004 when the railroad inked two more deals, one to move tires for Les Schwab Tire Company and the other to purchase the Crooked River Dinner Train. Some of these advances have been short lived, however, as L-P has since closed the Hines plant and the dinner train ceased operations in late 2008. The dinner train remained closed for only a short time, however, as a private party stepped in to take it over. Unfortunately, the private party could not make a go of the operation either and soon ceased operations. The railroad sold the two dining cars in November 2011 to the Mt. Rainier Scenic Railroad of Mineral, Washington, which has eliminated regular passenger service from the railroad.

The City of Prineville continues to be one of the oldest municipally built and operated railroads in the United States. The railroad has reshaped itself into a distribution center serving all of central and eastern Oregon, with most freight passing through two reload centers. The original reload at the Prineville Freight Depot ships and receives a wide variety of products, while bulk and liquid products move through a second reload the company built at Prineville Junction. The company generates additional substantial revenues through commercial car storage on the many idled industrial spurs and sidings. The railroad has successfully pursued additional grant monies to upgrade its track structure, and the company is now back on a firm financial footing. The Mt. Emily Shay remained on the property and operated a couple times a year for passenger excursions or other civic events until 1 September 2022 when the Oregon Historical Society conveyed the locomotive to the Oregon Rail Heritage Foundation, which moved it to the Oregon Rail Heritage Center in Portland, Oregon, at the end of 2023.