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Ockford joined USL Championship team Louisville City FC on a full-time basis on December 5, 2019.

On January 10, 2017, it was announced that USL side and San Jose Earthquakes affiliate Reno 1868 FC had signed Ockford. He scored his first goal for the team on May 20, 2017, in Reno's 6–0 rout of his former team Seattle Sounders FC 2. Ockford made his first appearance for San Jose as a 33rd-minute substitute for Andrés Imperiale on July 14, 2017, during San Jose's 4–1 friendly victory over Eintracht Frankfurt.

Ockford was signed by the San Jose Earthquakes on December 14, 2017, along with Reno teammates Chris Wehan and Luis Felipe Fernandes. He made his MLS debut on March 3, 2018, during San Jose's season-opening 3–2 victory over Minnesota United, substituting on in the 54th minute after Yeferson Quintana was injured.

On January 16, 2014, Ockford was drafted in the second round of the 2014 MLS SuperDraft (21st overall) by Seattle Sounders FC. He signed with the club on February 26 and was immediately loaned to NASL club New York Cosmos. On May 28, Ockford made his professional debut and scored his first goal in a 2–0 win over NPSL club Brooklyn Italians in the third round of the Lamar Hunt U.S. Open Cup. Three days later, he made his NASL debut and scored in a 3–0 win against Fort Lauderdale Strikers.

Ockford scored two goals and made 10 appearances for the Cosmos during the 2014 regular season, helping the team clinch a berth in The Championship. He also scored one goal in three U.S. Open Cup appearances for the Cosmos.

On February 6, 2013, it was announced that Ockford transferred to the University of Louisville for his senior season. In his lone season with the Cardinals, Ockford was converted to defender and he excelled as he made 20 appearances, tallied four goals and helped the Cardinals record nine clean sheets on their way to winning the AAC regular season title. On November 14, Ockford was named AAC Defender of the Year.

Ockford began his college career at Mount St. Mary's University where he played as a forward for three seasons. In his freshman year with the Mountaineers, Ockford made 17 appearances and finished the year with one assist. In 2011, he made 16 appearances and tallied three goals and three assists. In 2012, he made 17 appearances and tallied two goals. Following the conclusion of the 2012, Mount St. Mary's Athletics announced that it would cut three of their sports programs, including men's soccer.

James William Ockford (born June 10, 1992) is an American soccer player who plays for Louisville City FC in the USL Championship.