Qualifying took place over four days and was marked by an unusual start. On pole day, Saturday May 14, most competitors agreed informally to sit out the gusty conditions and qualify together the following day. Jerry Hoyt was not informed of the arrangement and launched an unexpected qualifying attempt in the final 20 minutes, posting a speed of 140.045 mph that was slow by the day's standards but sufficient to claim the provisional pole. Tony Bettenhausen Sr. followed but could not better Hoyt's time for pole position. Hoyt's pole speed ultimately ranked only eighth overall in the field — the slowest ranked pole speed in Indy history to that point. The fastest overall qualifier was Jack McGrath at 142.580 mph, who lined up third on the grid.
During the second day of qualifying, Manny Ayulo crashed due to a suspected steering fault and died the following day, casting a shadow over the start of the month.
Jack McGrath led from the outside of the front row at the start but was quickly challenged by Vukovich. Vukovich assumed the lead on lap four and traded it back and forth with McGrath through the early laps. McGrath retired on lap 54 with a magneto failure, leaving Vukovich in command with a considerable cushion.
On lap 56, with Vukovich leading by a wide margin, a multi-car incident unfolded ahead of him. Rodger Ward, several laps down, spun and came to rest facing the wrong direction. Al Keller swerved to avoid Ward, drifting onto the infield grass before swinging back up the track and striking Johnny Boyd. Boyd's car was deflected into the path of Vukovich, who appeared to be moving left to avoid Ward. A last-second right-hand correction could not prevent contact; Boyd's car launched Vukovich's machine hard into the outside barrier. The front end cleared the wall and the car cartwheeled, striking vehicles parked outside the circuit and possibly a pole. The car came to rest on fire. Vukovich died from a skull fracture. Boyd and the other involved drivers escaped serious injury. Driver Ed Elisian stopped his car on the infield grass and ran across the track in an attempt to help.
After a 27-minute caution period, Jimmy Bryan led before retiring with a fuel pump issue at lap 90. Bob Sweikert then took over and led the majority of the remaining distance. Art Cross led from laps 133 to 156 and Don Freeland held the lead briefly before both retired with mechanical problems. Sweikert drove the final miles unopposed, winning his first and only Indianapolis 500.
Bob Sweikert's victory completed a remarkable triple: he also won the 1955 AAA National Championship and the 1955 Midwest Sprint Car championship, making him the only driver in history to sweep all three titles in a single season.
The race was part of an exceptionally deadly year for global motorsport, which also saw Alberto Ascari killed testing at Monza and nearly 100 fatalities at the 24 Hours of Le Mans disaster involving Pierre Levegh. In the aftermath of 1955, the American Automobile Association withdrew from sanctioning motorsport. The United States Auto Club was formed to take over sanctioning duties beginning in 1956. The carnage of the season also accelerated discussions about driver safety that would eventually lead to mandatory fire suits in 1959.
The race also marked the final appearance of a front-drive car at Indianapolis: Paul Russo, attempting to qualify the Novi for Troy Ruttman, suffered a broken gearbox during the third qualifying day.