diff --git a/.github/workflows/gen-openapi.yml b/.github/workflows/openapi.yml
similarity index 96%
rename from .github/workflows/gen-openapi.yml
rename to .github/workflows/openapi.yml
index bd66644e..ea88978a 100644
--- a/.github/workflows/gen-openapi.yml
+++ b/.github/workflows/openapi.yml
@@ -78,13 +78,12 @@ jobs:
             sleep 2
           done
 
-      - name: Run app
+      - name: Run generator
         env:
           DATABASE_URL: postgres://zipline:zipline@localhost:5432/zipline
           CORE_SECRET: ${{ steps.secret.outputs.secret }}
-          ZIPLINE_OUTPUT_OPENAPI: true
-
-        run: pnpm start
+          NODE_ENV: production
+        run: pnpm openapi
 
       - name: Verify openapi.json exists
         run: |
diff --git a/package.json b/package.json
index 1fc1d62c..d1a976d6 100644
--- a/package.json
+++ b/package.json
@@ -12,6 +12,7 @@
     "start:inspector": "cross-env NODE_ENV=production node --require dotenv/config --inspect=0.0.0.0:9229 --enable-source-maps ./build/server",
     "ctl": "NODE_ENV=production node --require dotenv/config --enable-source-maps ./build/ctl",
     "validate": "tsx scripts/validate.ts",
+    "openapi": "tsx scripts/openapi.ts",
     "db:prototype": "prisma db push --skip-generate && prisma generate --no-hints",
     "db:migrate": "prisma migrate dev --create-only",
     "docker:engine": "colima start --mount $PWD/themes:w --mount $PWD/uploads:w --mount $PWD/public:w",
diff --git a/scripts/index.ts b/scripts/index.ts
index 78a18304..37b83a69 100644
--- a/scripts/index.ts
+++ b/scripts/index.ts
@@ -1,4 +1,6 @@
-export function step(name: string, command: string, condition: () => boolean = () => true) {
+type StepCommand = string | (() => void | Promise<void>);
+
+export function step(name: string, command: StepCommand, condition: () => boolean = () => true) {
   return {
     name,
     command,
@@ -35,7 +37,11 @@ export async function run(name: string, ...steps: Step[]) {
 
     try {
       log(`> Running step "${name}/${step.name}"...`);
-      execSync(step.command, { stdio: 'inherit' });
+      if (typeof step.command === 'string') {
+        execSync(step.command, { stdio: 'inherit' });
+      } else {
+        await step.command();
+      }
     } catch {
       console.error(`x Step "${name}/${step.name}" failed.`);
       process.exit(1);
diff --git a/scripts/openapi.ts b/scripts/openapi.ts
new file mode 100644
index 00000000..e8898735
--- /dev/null
+++ b/scripts/openapi.ts
@@ -0,0 +1,110 @@
+import { readFile, writeFile } from 'fs/promises';
+import path from 'path';
+import { run, step } from '.';
+import { API_ERRORS, ApiError, ApiErrorCode } from '../src/lib/api/errors';
+
+const ALL_METHODS = ['delete', 'get', 'head', 'patch', 'post', 'put'];
+const GEN_PATH = path.resolve(__dirname, '..', 'openapi.json');
+
+const ALL_ERRORS = Object.keys(API_ERRORS)
+  .map((code) => new ApiError(Number(code) as ApiErrorCode).toJSON())
+  .sort((a, b) => a.code - b.code);
+
+const ERROR_SCHEMA = {
+  type: 'object',
+  description: 'Generic error for API endpoints.',
+  properties: {
+    error: {
+      type: 'string',
+      description:
+        'Message for the error. This may differ from the standard message for the error code, but the error code should be used to figure out the type of error.',
+    },
+    code: {
+      type: 'integer',
+      format: 'int32',
+      description:
+        'Zipline API error code. Ranges: 1xxx validation, 2xxx session, 3xxx permission, 4xxx not-found, 5xxx constraint, 6xxx internal, 9xxx generic.',
+      enum: ALL_ERRORS.map((entry) => entry.code),
+      'x-enumDescriptions': ALL_ERRORS.map((entry) => entry.message),
+    },
+    statusCode: {
+      type: 'integer',
+      format: 'int32',
+      description: 'HTTP status code returned alongside this error payload.',
+    },
+  },
+  required: ['error', 'code', 'statusCode'],
+  additionalProperties: true,
+};
+
+const ERROR_EXAMPLES = ALL_ERRORS.reduce<Record<string, unknown>>((examples, entry) => {
+  examples[`E${entry.code}`] = {
+    summary: `${entry.error}`,
+    value: entry,
+  };
+
+  return examples;
+}, {});
+
+const generic4xxResponse = {
+  description: 'API error response (4xx)',
+  content: {
+    'application/json': {
+      schema: ERROR_SCHEMA,
+      examples: ERROR_EXAMPLES,
+    },
+  },
+};
+
+function addErrorResponse(responses: Record<string, any>): void {
+  const response = (responses['4xx'] ??= structuredClone(generic4xxResponse));
+
+  response.description ??= generic4xxResponse.description;
+  response.content ??= {};
+
+  const jsonContent = (response.content['application/json'] ??= {});
+  jsonContent.schema ??= structuredClone(ERROR_SCHEMA);
+  jsonContent.examples ??= structuredClone(generic4xxResponse.content['application/json'].examples);
+}
+
+function filterRoutes(paths = {}): Record<string, any> {
+  return Object.fromEntries(Object.entries(paths).filter(([route]) => route.startsWith('/api')));
+}
+
+async function fixSpec() {
+  const spec = JSON.parse(await readFile(GEN_PATH, 'utf8'));
+
+  spec.paths = filterRoutes(spec.paths);
+
+  for (const [, pathItem] of Object.entries(spec.paths ?? {})) {
+    if (!pathItem) continue;
+
+    for (const method of ALL_METHODS) {
+      const operation = (<any>pathItem)[method];
+      if (!operation) continue;
+
+      operation.responses ??= {};
+      addErrorResponse(operation.responses);
+    }
+  }
+
+  await writeFile(GEN_PATH, JSON.stringify(spec));
+}
+
+process.env.ZIPLINE_OUTPUT_OPENAPI = 'true';
+
+run(
+  'openapi',
+  step('run-prod', 'pnpm start', () => process.env.NODE_ENV === 'production'),
+  step('run-dev', 'pnpm dev', () => process.env.NODE_ENV !== 'production'),
+  step('check', async () => {
+    try {
+      await readFile(GEN_PATH);
+    } catch (e) {
+      console.error('\nSomething went wrong...', e);
+
+      throw new Error('No OpenAPI spec found at ./openapi.json');
+    }
+  }),
+  step('fix', fixSpec),
+);
diff --git a/src/lib/api/errors.ts b/src/lib/api/errors.ts
index 81add390..cfafc86a 100644
--- a/src/lib/api/errors.ts
+++ b/src/lib/api/errors.ts
@@ -148,7 +148,7 @@ export class ApiError extends Error {
 
   toJSON(): ApiErrorPayload {
     const formattedMessage = API_ERRORS[this.code]
-      ? `${this.code}${this.message ? `: ${this.message}` : ''}`
+      ? `E${this.code}${this.message ? `: ${this.message}` : ''}`
       : this.message;
 
     return {
@@ -163,7 +163,7 @@ export class ApiError extends Error {
     return payload.code === code;
   }
 
-  private static codeToHttpStatus(code: ApiErrorCode): number {
+  public static codeToHttpStatus(code: ApiErrorCode): number {
     const override = {
       9000: 400,
       9001: 403,