Imidacloprid is a neonicotinoid neurotoxin that remains the most used insecticide worldwide. It persists in the environment long after the initial application resulting in chronic exposure to non-target insects. To accurately map the dose-dependent effects of these exposures across taxa, toxicological assays need to assess various modes of exposure across relevant indicator species. However, due to the difficulty of these experiments, contact bioassays are frequently used to quantify dose, and dipterans remain underrepresented. Here, we developed a novel naturalistic feeding bioassay to precisely measure imidacloprid ingestion and its toxicity for acute and chronic exposures in a dipteran pollinator, Eristalis tenax. Flies which ingested imidacloprid dosages lower than 12.1 ng/mg all showed consistent intake volumes and learned improved feeding efficiency over successive feeding sessions. In contrast, at doses of 12.1 ng/mg and higher flies had a rapid onset of severe locomotive impairment which prevented them from completing the feeding task. Neither probability of survival nor severe locomotive impairment were significantly higher than the control group until doses of 1.43 ng/mg or higher were reached. We were unable to measure a median lethal dose for acute exposure (72 hours) due to flies possessing a relatively high tolerance for imidacloprid. However, with chronic exposure (18 days), mortality went up and an LD50 of 0.41 ng/mg was estimated. Severe locomotive impairment tended to occur earlier and at lower dosages than lethality, with ED50s of 0.17 ng/mg and 7.82 ng/mg for acute and chronic exposure, respectively. Although the adult Eristalis is a honeybee mimic, it possesses a much higher tolerance to this toxin than its model. The similarity in the LD50 to other dipterans such as the fruitfly and the housefly suggests that there may be a phylogenetic component to pesticide tolerance that needs to be further investigated. The absence of obvious adverse effects at sublethal dosages also underscores a need to develop better tools for quantifying animal behaviour to evaluate the impact of insecticides on foraging efficiency in economically important species.