On a hot, sweltering day, a train jumps the tracks outside Medicine Bend. Murray Sinclair answers the call with his loyal crew and starts work on cleaning up the tracks, while heavily looting the goods from the wreck. A tramp, known as Wickwire, is injured in the wreckage, but Sinclair refuses to allow his men to offer water to the dying man, and leaves him for dead. When George McCloud, the line’s new superintendent, arrives, he and Sinclair start fighting about Sinclair’s looting. Sinclair rallies his men to strike, holding his ground against McCloud and his orders to return all the stolen goods. McCloud, unrelenting to Sinclair’s pressures, fires the men on spot, which sparks the beginning of a war between Sinclair and the railroad.
In order to speed up the wreckage cleaning, McCloud lights the train on fire, which captures the attention of Dicksie Dunning, who is riding back home from a visit to Medicine Bend. Dicksie, the owner of the Crawling Stone Ranch along with her cousin, Lance Dunning, spots the fire and arrives to offer her assistance. Upon first sight, McCloud is instantly smitten, and urges her to stay longer and give her horse water and rest. Midway in their conversation, they spot Wickwire, and send him off to the Barnhardt, the railroad surgeon down in Medicine Bend.
After the town hears about Sinclair’s firing, they rally in support for him to get his job back. However, the railroad company, tired of Sinclair’s looting, refuses to yield, telling Sinclair how many opportunities he’s had to change his ways. Sinclair takes the blow hard and starts crying and cursing during the meeting. Eventually Farrell Kennedy, the chief of special services for the railroad, escorts him out of the Wickiup, the local headquarters for the company. Sinclair blames McCloud for his firing, ignoring his own thieving role as a factor, and vows his revenge against those he feels betrayed him.
The next time he’s in town, he visits his estranged wife, Marion Sinclair, at her millinery shop, where he runs into McCloud. Sinclair threatens McCloud and tells him to leave town. Marion, who left Sinclair due to his drinking and unruly behavior, embarrassedly escorts him out the door. She is more than well aware of her husband’s temper, and as a good friend of McCloud, who rents a room from her, becomes entangled in Sinclair’s fight. When McCloud retreats to his office after the encounter with Sinclair, he hears about the Smokey Creek Bridge fire, which causes havoc for the line.
McCloud diligently tries to clean up the mess caused by the bridge’s destruction, which is presumably the result of Sinclair’s revenge. However, he encounters the backlash of Lance Dunning, Dicksie’s cousin. Lance is upset that his cattle were misplaced during the commotion after the fire, and worried they might catch a disease in their new holding place; he lashes out at McCloud for mishandling the situation. Lance is a good friend of Sinclair, as they grew up together learning how to build bridges from Lance’s uncle, Richard Dunning, who is also Dicksie’s father. In the battle between the railroad company and Sinclair, Lance takes Sinclair’s side, and uses the Smokey Creek Bridge fire as an opportunity to flaunt his loyalties. Dicksie shares her older cousin’s sentiments, as she bad-mouths McCloud to Marion, her best friend. However, Dicksie, who is highly sheltered, losing both her parents at a young age, and after going away to boarding school during her schooling years, only knows the ranch and the men on it, who have all taken Sinclair’s side. When McCloud accidently overhears her insults, he is hurt, but also aware that she speaks from the same point of view as the mountain men Sinclair represents.
After the bridge fire, there is a quick succession of disasters affecting the railway. Another train wreck occurs, except this time there is evidence of foul play at the site. Ten days later, a train is robbed at gunpoint at the Sugar Buttes station outside of Sleepy Cat town. The robbers, led by Sinclair, shoot and kill Sleepy Cat’s Sheriff Van Horn, and steal off with the train’s gold. After hearing of these occurrences, President Bucks, owner of the railroad company, sends his lawman, Gordon Smith, into town.
Gordon Smith, the man, is not nearly as famous as his moniker, Whispering Smith, the lawman. His reputation precedes him, as the fastest draw, the quickest fire, and the undefeated. Whispering Smith arrives and is consulting with McCloud when Bill Dancing, the company’s lineman, comes in to suggest a truce between McCloud and Sinclair. Ironically, unbeknownst to Bill is Sinclair’s role in the recent attacks, and Whispering Smith’s identity. Whispering Smith values Bill’s ignorance as an opportunity to initiate communication between the railroad and Sinclair, and offers enthusiastic support of Bill’s idea. When Bill races over to tell Sinclair the news, Sinclair successfully identifies Whispering Smith as the stranger in Bill’s story.
Winter approaches Medicine Bend. However, President Bucks orders the company to keep installing new tracks, further jeopardizing the company’s reputation in the town. Headed by McCloud, the men work tirelessly on Christmas Day to continue laying tracks down for the new line, when a freak blizzard hurtles toward them. McCloud takes the reins of the situation and has the men quickly set a new pair of tracks in order to make a three-point turn to safety and quickly head back into town. His tricky maneuver earned him the much-needed respect of the men and the town, except for Lance Dunning, who calls McCloud over to the Crawling Stone Ranch to dispute the railroad’s rights of passage through Crawling Stone. Lance, still under the influence of Sinclair, tells McCloud of his new decision to build an irrigation system in the same location the railroad would pass. McCloud immediately reminds Lance of the company’s rights of passage, which Lance consented to, and the two starting fighting. Dicksie, overhearing the argument, intervenes to prevent the fight from escalating.
Dicksie waits for McCloud to leave the ranch before warning him of his enemies in the land. McCloud, jumping at the opportunity to spend time with Dicksie, convinces her to let him ride her back to her ranch, and the two finally get a chance to talk one on one. As McCloud heads back to Medicine Bend, a shot is fired, hitting his hat mere inches from his head. McCloud frantically races back to Medicine Bend to tell Whispering Smith about what happened. However, Whispering Smith, two steps ahead of everything, already knew, and makes a plan with McCloud and Farrell Kennedy to track the shooter, the albino Harvey Du Sang, down.
Harvey Du Sang’s reputation with a gun equals that of Whispering Smith; however, his ability stems from a life of breaking the law, rather than protecting it. As Sinclair’s right-hand man, Du Sang proves to be just as conniving as his boss. Whispering Smith tracks Du Sang to a dive on the outskirts of town, and pins him inside with Farrell on the left and McCloud on the right. Du Sang, nervous of his chances in a shootout, slinks against the wall as Whispering Smith tells him to leave town or be dragged through it. As they leave the establishment, successful in their attempt to scare Du Sang, Whispering Smith warns McCloud to hide his hat, so Du Sang won’t know how close to a kill he got.
As winter comes to an end, McCloud patiently sits in his office as Callahan, who oversees the Overland section of the railroad, informs him that Lance Dunning went to the courts to get an injunction, effectively locking the company in a year-long battle over the right-of-way passage through Crawling Stone. This hinders all the work McCloud has placed into setting the new line up, but nevertheless, he sets himself to work on smoothing out the current line. The weather unleashes a nasty flood that hits Crawling Stone the hardest. Lance desperately tries to salvage the land with the help of Sinclair and his men, but to no avail. Dicksie, watching the madness circling around her, calls on Marion for guidance. Marion suggests that McCloud could help, but Dicksie, afraid of the mistreatment he has received from Lance, fears he won’t oblige. After much cajoling, Marion convinces Dicksie to ask McCloud for help, and they set out to the campsite where McCloud and his men have successfully fought off the flooding.
When they arrive, McCloud immediately offers his assistance, along with one hundred of his men, and then Whispering Smith shows up unannounced. For the first time, the four were able to talk, and while they dined, Whispering Smith alleviated Dicksie’s nervousness with a poem about trouble, much to everyone’s pleasure. After dinner, Dicksie follows Whispering Smith outside and spends the night talking to the man she’s heard so many ugly rumors about. In the morning, the four ride out to Crawling Stone ranch much to Lance’s astonishment and set to work wrangling the flood back in. During a break in the heavy commotion, Whispering Smith briefly warns Dicksie about Sinclair’s involvement in the robberies and attacks. He spells out the possible danger this brings to Marion, and Dicksie promises to protect her from Sinclair’s impending advances. A day later, Dicksie finds herself at Sinclair’s ranch, the Frenchman, watching over Marion and Sinclair’s conversation. Sinclair appeals to Marion to leave town with him, which she adamantly refuses to do. Desperate, he threatens to kill Marion on the spot, who, in response, simply sits there undeterred, until he gets up, leaving her by herself.
Later that night, Whispering Smith is sitting alone in his room, when he hears a knock at his door. He opens it to find McCloud and Farrell standing there with the news of a second train robbery at the Tower W station, with one reported dead, one injury, and an empty safe. Quickly, Whispering Smith grabs his gear while shouting out instructions. The three men head out to an empty train waiting to take them to the crime scene. Once there, they follow the tracks of the outlaws until they disappear under a stampede of new ones. Immediately, they sniff out a cover-up and find a horse rancher named Rockstro who admits to covering the tracks with his horses for a fee. Instead of turning the man over for a prior crime, Whispering Smith lets Rockstro off, in gratitude for the information, and splits his crew up in search of the robbers.
The robbers, led by Du Sang in Sinclair’s absence, runs into one of Whispering Smith’s posses led by Medicine Bend’s Sheriff Ed Banks. They find the home of Dan Baggs, a retired locomotive engineer, who lives alone with his ten-year-old son, Dannie. Sheriff Banks already warned Baggs of the danger they faced, but Baggs is unable to successfully identify Du Sang and his gang when they arrive. Du Sang kills Baggs and takes off with one of his horses. When Sheriff Banks tracks back to his house, he finds Dannie crying over his father’s dead body. That night Whispering Smith comforts the orphaned boy, while his group heals from the grueling journey.
Whispering Smith tracks Du Sang back to Williams Cache, an infamous hideout for many outlaws of the land. John Rebstock acts as patriarch for the Cache, collecting rent money from the men he protects. After some convincing, Whispering Smith finally talks to Rebstock about Du Sang’s release, which Rebstock refuses. Fed up with the talks, Whispering Smith orders a roundup of the Cache, which includes collecting any illegally owned cattle and their outlaw owners to force Du Sang out. On the day of the roundup, Whispering Smith and his gang break off into groups, attacking the Cache at all entrances. In the late afternoon, Whispering Smith, with four other riders, faces Du Sang and two men in a shootout. One of Whispering Smith’s men takes a hit, while the others flee for their lives, leaving Whispering Smith to face Du Sang and his crew alone. Whispering Smith throws himself down off his horse, catching his rifle in his fall, and successfully shoots the men down. After the fight, he attends to his fallen man, Bill Dancing, while the others come back to hang the fallen outlaws. Whispering Smith puts an end to the hanging, and finds Du Sang injured on the side of a hill. Whispering Smith takes Du Sang back to Rebstock, who refuses to allow him entrance into his cabin, so they stash him in the barn. Later on that evening, Du Sang yells Whispering Smith’s name just before dying.
Back in Medicine Bend, McCloud, Dicksie, and Marion anxiously await news of Whispering Smith’s condition after the shootout, until they receive a wire from Whispering Smith himself. Relieved that Whispering Smith made it through uninjured, the three are celebrating over lunch, when Smith arrives at Marion’s door, causing a second wave of celebration. After dinner, McCloud and Dicksie escape for a private chat outside, and Whispering Smith conspires with Marion to trick them into admitting they are starting a relationship with each other. Later on that night, after everyone retires, Marion gets an unexpected knock at her door. Sinclair tries again to convince Marion to go away with him, to which she steadfastly refuses. In frustration, he blames Whispering Smith for her decision, claiming the two are secretly in love with each other. Insulted at his claims, Marion turns him away, and he threatens to avenge his grievances against both Whispering Smith and McCloud.
Two days later, President Bucks arrives to talk with Whispering Smith and McCloud about the recent events. During their conversation, a messenger informs the trio that Sheriff Ed Banks was shot trying to serve Sinclair the warrants for his arrest. As Banks lies bleeding, he bequeaths the responsibility of serving Sinclair to Whispering Smith. Marion, aware of the new report, blames herself for Sinclair’s behavior, and unsure of what to do, confers with Dicksie and McCloud. When the two leave for a walk, Marion finds herself alone with Whispering Smith who wants to know whether he should kill Sinclair or be killed by him. The love between the two is palpable as Marion fights her emotions: she doesn’t want any harm to come to her estranged husband, but she couldn’t allow Whispering Smith to die for him. With this understanding, Whispering Smith heads back to his room to prepare for the long trek. On his way, Wickwire, the tramp from the first train wreck, stops to ask him if he can assist Whispering Smith on his journey. Wickwire, still angry with Sinclair for leaving him to die, wants his own revenge, which Whispering Smith doesn’t deny.
That night, as Smith gets ready, he tells McCloud about growing up with Sinclair in the same small town. Whispering Smith idolized Sinclair as a boy, looking up to him as a man and a hero. The revelation of his relationship with Sinclair illustrates the hesitancy Whispering Smith has in taking him down. Whispering Smith never meant to face Sinclair in a duel because despite his actions, he respects the boy he once knew and the husband he is. With a last embrace from McCloud, Whispering Smith heads north to track Sinclair down.
Smith travels to Oroville, where he knows Sinclair is hiding out after successfully freeing one of his men who was involved in the Williams Cache shootout. However, before Whispering Smith could go looking for Sinclair, he is blocked by three men from the Williams Cache roundup, looking to make even on their lost cattle. Again, Whispering Smith is caught in a tricky and potentially life-threatening situation, and again Smith pulls a sneaky trick on the men to get his gun into his hands. Whispering Smith lets two of the men go, but apprehends the leader, Fatty Filber, who is wanted for cattle thieving in another county. While Whispering Smith is held up in Oroville, Sinclair rides to Lance Dunning’s house for some friendly comfort as he slowly loses control and support from those around him. Lance sympathetically listens to Sinclair speak as a storm brews outside. Sinclair tells him his plan to ride back into Medicine Bend to pick up his wife and settle his scores with the railroad. Dicksie, who had arrived home after spending some time in Medicine Bend earlier in the day, overhears Lance with Sinclair, and waits for an opportunity to alert McCloud and Marion of his intentions. When Lance walks Sinclair out, Dicksie runs for the phone that won’t work because of the terrible weather. Dicksie faces off with Lance, upset that he let Sinclair go, and gets her horse ready to ride into town to protect her friends.
Dicksie rides throughout the storm, pounded with rain, sleet, and snow. As she rides, she passes another rider, presumably Sinclair, and continues on farther and harder. By the ride’s end, she is barely conscious, constantly slipping out of her saddle until she lands, knocked out, at Marion’s door. She comes to in enough time to tell Marion and Barnhardt of Sinclair’s intentions before Sinclair comes knocking on the door. Barnhardt answers the door and tells Sinclair to leave town under cover of the storm and never to return, since he’s lost most of the support in the town. Sinclair leaves, right after breaking into McCloud’s office, to find that McCloud is two hundred miles away on a work trip. Whispering Smith arrives at Marion’s after hearing news of the incident, and helps to calm Marion and Dicksie down. Unfortunately, Whispering Smith knows his job isn’t done, since Sinclair is searching for the money left over from the Tower W robbery; however, what Sinclair doesn’t know is that Farrell Kennedy took that money during the Williams Cache roundup, leaving Whispering Smith with more time to catch him.
Whispering Smith and Wickwire, along Kennedy and another man, travel through the mountains in search of Sinclair. Whispering Smith and Wickwire split up to follow a trail they believe to be Sinclair’s. While traversing through a dangerous wash, they spot Sinclair with two other men. Whispering Smith, already hiding in the wash, shoots at one man, while Wickwire riding above the wash, shoots at Sinclair and his partner. It takes Wickwire only one shot to kill Sinclair and his partner.
In the year since Sinclair’s death, Whispering Smith left Medicine Bend and had not been heard from during that time. Dicksie and McCloud married, and the railroad company successfully built a line through Crawling Stone Ranch without any further problems. On one fateful afternoon, McCloud arrives back in town with news that Whispering Smith is sick in a hospital with typhoid fever. Marion immediately packs up to attend to Whispering Smith and bring him back to Medicine Bend to recover. When Whispering Smith and Marion reunite for the first time since the death of her husband, Whispering Smith tells Marion that he loves her. Marion, who knew that from the look in his eyes, tells him how happy she is to finally hear it from his mouth.