The Locust Hill Country Club originated in the summer of 1925 by thirty of the younger and more progressive business and professional men of Rochester and members of the Rochester Gyro club. They purchased from Frank Zornow the "Locust Hill Farm" - eighty-nine acres of farm land on the north side of Jefferson Road in Pittsford. The barn was converted into a Locker House, with a fully equipped Pro Shop, bag storage, showers, lockers, and lounge room where food was served. The farm house was made into the clubhouse with 40 lockers on the second floor for the lady players. The course initially featured nine excellent holes for golf.

The Club soon expanded to 225 members and in 1927 purchased 52 acres South of Jefferson Road. It expanded to eighteen holes following the same careful procedure as before, taking in the additional members required for financing the expansion, with these  new members being allowed to extend their payments over a period of two years.

That same year, Silk Callahan was hired as the head Golf Pro with Harry Boyce the Head Greens Keeper and George Pappart as Club Manager.

Golfing at Locust Hill hummed along smoothly until December 24, 1936, when a clubhouse fire destroyed the facility. The bartender living in the building lost his life. Forty women's lockers were destroyed. While the cause of the fire was undetermined, the Pittsford Fire Chief said it started around the furnace.

In 1946, Joe LaMachia became head pro. In 1949, an irrigation system was installed to water the fairways and greens.

The club built a two story building behind the clubhouse in 1967 to house the men's locker room, pro shop, and golf cart storage.

In 1984 the clubhouse underwent a $1 million dollar renovation that connected the main clubhouse and the locker room building with the addition of the main members dining room on the main level. A patio off the dining room was enclosed to create a separate bar area in 1991. The clubhouse received a complete $3million interior renovation in 1998 which included the addition of the three-story octogon "Loggia".  The master plan for the clubhouse was completed in 2006 with an addition to the ballroom, a 2,000 state-of-the-art fitness center, and exterior decks and patios overlooking the golf course.

Locust Hill is the home of the Wegman's Rochester International, an annual event on the LPGA Tour. The LPGA has competed on Locust Hill's championship course every year since 1977.