diff --git a/src/components/Input.js b/src/components/Input.js
index 0bec7bcf..4d8ff262 100644
--- a/src/components/Input.js
+++ b/src/components/Input.js
@@ -5,7 +5,7 @@ import { color, typography, spacing } from './shared/styles';
 import { jiggle } from './shared/animation';
 import { Icon } from './Icon';
 import { Link } from './Link';
-import WithTooltip from './tooltip/WithTooltip';
+import WithTooltip, { validPlacements as validTooltipPlacements } from './tooltip/WithTooltip';
 import { TooltipMessage } from './tooltip/TooltipMessage';
 
 // prettier-ignore
@@ -268,6 +268,7 @@ export const PureInput = forwardRef(
       icon,
       error,
       appearance,
+      errorTooltipPlacement,
       className,
       lastErrorValue,
       startingType,
@@ -327,7 +328,7 @@ export const PureInput = forwardRef(
           */}
           <ErrorTooltip
             tabIndex={-1}
-            placement="right"
+            placement={errorTooltipPlacement}
             trigger="none"
             startOpen
             tagName="div"
@@ -357,6 +358,7 @@ PureInput.propTypes = {
   id: PropTypes.string.isRequired,
   value: PropTypes.string,
   appearance: PropTypes.oneOf(['default', 'secondary', 'tertiary', 'pill', 'code']),
+  errorTooltipPlacement: PropTypes.oneOf(validTooltipPlacements),
   stackLevel: PropTypes.oneOf(['top', 'middle', 'bottom']),
   label: PropTypes.string.isRequired,
   hideLabel: PropTypes.bool,
@@ -374,6 +376,7 @@ PureInput.propTypes = {
 PureInput.defaultProps = {
   value: '',
   appearance: 'default',
+  errorTooltipPlacement: 'right',
   stackLevel: undefined,
   hideLabel: false,
   orientation: 'vertical',
diff --git a/src/components/Input.stories.js b/src/components/Input.stories.js
index eb8abd79..05d3c665 100644
--- a/src/components/Input.stories.js
+++ b/src/components/Input.stories.js
@@ -140,6 +140,7 @@ const All = ({ appearance }) => (
       placeholder="Error with icon"
       icon="email"
       error="There's a snake in my boots"
+      errorTooltipPlacement="left"
       onChange={onChange}
       appearance={appearance}
     />
diff --git a/src/components/tooltip/WithTooltip.js b/src/components/tooltip/WithTooltip.js
index eb908e57..9aeb5e6a 100644
--- a/src/components/tooltip/WithTooltip.js
+++ b/src/components/tooltip/WithTooltip.js
@@ -169,11 +169,17 @@ function WithTooltip({
   );
 }
 
+const placementVariations = ['start', 'end'];
+export const validPlacements = ['auto', 'top', 'right', 'left', 'bottom'].flatMap((placement) => [
+  placement,
+  ...placementVariations.map((variation) => `${placement}-${variation}`),
+]);
+
 WithTooltip.propTypes = {
   tagName: PropTypes.string,
   trigger: PropTypes.string,
   closeOnClick: PropTypes.bool,
-  placement: PropTypes.string,
+  placement: PropTypes.oneOf(validPlacements),
   modifiers: PropTypes.shape({}),
   hasChrome: PropTypes.bool,
   tooltip: PropTypes.oneOfType([PropTypes.node, PropTypes.func]),