diff --git a/packages/insomnia-app/app/models/plugin-data.js b/packages/insomnia-app/app/models/plugin-data.js
index beebb3af9..0320d48fd 100644
--- a/packages/insomnia-app/app/models/plugin-data.js
+++ b/packages/insomnia-app/app/models/plugin-data.js
@@ -51,6 +51,10 @@ export async function removeByKey(plugin: string, key: string): Promise<void> {
   return db.removeWhere(type, { plugin, key });
 }
 
+export async function removeAll(plugin: string): Promise<void> {
+  return db.removeWhere(type, { plugin });
+}
+
 export async function getByKey(
   plugin: string,
   key: string
diff --git a/packages/insomnia-app/app/plugins/context/store.js b/packages/insomnia-app/app/plugins/context/store.js
index 6661975fa..402ad799b 100644
--- a/packages/insomnia-app/app/plugins/context/store.js
+++ b/packages/insomnia-app/app/plugins/context/store.js
@@ -18,6 +18,9 @@ export function init(plugin: Plugin) {
       },
       async removeItem(key: string): Promise<void> {
         await models.pluginData.removeByKey(plugin.name, key);
+      },
+      async clear(key: string): Promise<void> {
+        await models.pluginData.removeAll(plugin.name);
       }
     }
   };
diff --git a/plugins/insomnia-plugin-prompt/index.js b/plugins/insomnia-plugin-prompt/index.js
index 4f0b79b41..901a65e64 100644
--- a/plugins/insomnia-plugin-prompt/index.js
+++ b/plugins/insomnia-plugin-prompt/index.js
@@ -1,4 +1,12 @@
-const STORE = {};
+module.exports.responseHooks = [
+  context => {
+    const requestId = context.response.getRequestId();
+
+    // Delete cached value so it will prompt again on the next request
+    context.store.removeItem(requestId);
+  }
+];
+
 module.exports.templateTags = [
   {
     displayName: 'Prompt',
@@ -30,10 +38,17 @@ module.exports.templateTags = [
           'something else.'
       }
     ],
-    async run(context, title, label, defaultValue, storageKey) {
-      if (STORE[storageKey]) {
+    async run(context, title, label, defaultValue, explicitStorageKey) {
+      // If we don't have a key, default to request ID.
+      // We do this because we may render the prompt multiple times per request.
+      // We cache it under the requestId so it only prompts once. We then clear
+      // the cache in a response hook when the request is sent.
+      const storageKey = explicitStorageKey || context.meta.requestId;
+      const cachedValue = await context.store.getItem(storageKey);
+
+      if (cachedValue) {
         console.log(`[prompt] Used cached value under ${storageKey}`);
-        return STORE[storageKey];
+        return cachedValue;
       }
 
       const value = await context.app.prompt(title || 'Enter Value', {
@@ -41,10 +56,9 @@ module.exports.templateTags = [
         defaultValue
       });
 
-      // Store if a key is set
       if (storageKey) {
         console.log(`[prompt] Stored value under ${storageKey}`);
-        STORE[storageKey] = value;
+        await context.store.setItem(storageKey, value);
       }
 
       return value;