On 12 November 2008, van der Werff made his FC Volendam debut in a 1–0 victory over Ajax in a KNVB Cup third round tie, replacing Marijn Sterk in the 87th minute.

On 30 January 2013, after impressing at FC Volendam, van der Werff joined PEC Zwolle on a two-and-a-half-year deal for a fee reported to be around the margin of £140,000.

On 30 March 2014, van der Werff scored his first PEC Zwolle goal in a 1–1 draw against ADO Den Haag, netting in the 21st minute.

[3] On 20 September 2015, van der Werff made his Vitesse debut in a 3–0 victory over local rivals De Graafschap, replacing Kevin Diks in the 27th minute.

He played as Vitesse won the final of the KNVB Cup 2–0 against AZ Alkmaar on 30 April 2017 to help the club, 3-time runners up, to the title for the first time in its 125-year history.