The experience of colour is a core element of human vision. Colours provide important symbolic and contextual information not conveyed by form alone. Moreover, the experience of colour can arise without external stimulation. For many people, visual memories are rich with colour imagery. In the unusual phenomenon of grapheme-colour synaesthesia, achromatic forms such as letters, words and numbers elicit vivid experiences of colour. Few studies, however, have examined the neural correlates of such internally generated colour experiences. We used functional magnetic resonance imaging (fMRI) to compare patterns of cortical activity for the perception of external coloured stimuli and internally generated colours in a group of grapheme-colour synaesthetes and matched non-synaesthetic controls. In a voluntary colour imagery task, both synaesthetes and non-synaesthetes made colour judgements on objects presented as grey scale photographs. In a synaesthetic colour task, we presented letters that elicited synaesthetic colours, and asked participants to perform a localisation task. We assessed the neural activity underpinning these two different forms of colour experience that occur in the absence of chromatic sensory input. In both synaesthetes and non-synaesthetes, voluntary colour imagery activated the colour-selective area, V4, in the right hemisphere. In contrast, the synaesthetic colour task resulted in unique activity for synaesthetes in the left medial lingual gyrus, an area previously implicated in tasks involving colour knowledge. Our data suggest that internally generated colour experiences recruit brain regions specialised for colour perception, with striking differences between voluntary colour imagery and synaesthetically induced colours.