diff --git a/roles/nginxplus/files/conf/http/allsearch-api_prod.conf b/roles/nginxplus/files/conf/http/allsearch-api_prod.conf
index b425755950..cb4161c036 100644
--- a/roles/nginxplus/files/conf/http/allsearch-api_prod.conf
+++ b/roles/nginxplus/files/conf/http/allsearch-api_prod.conf
@@ -51,5 +51,5 @@ server {
         proxy_cache allsearch-apicache;
     }
 
-    include /etc/nginx/conf.d/templates/errors.conf;
+    include /etc/nginx/conf.d/templates/errors-in-json-format.conf;
 }
diff --git a/roles/nginxplus/files/conf/http/allsearch-api_staging.conf b/roles/nginxplus/files/conf/http/allsearch-api_staging.conf
index cf97731711..5350e3a9f8 100644
--- a/roles/nginxplus/files/conf/http/allsearch-api_staging.conf
+++ b/roles/nginxplus/files/conf/http/allsearch-api_staging.conf
@@ -56,6 +56,5 @@ server {
         deny all;
     }
 
-    include /etc/nginx/conf.d/templates/errors.conf;
-
+    include /etc/nginx/conf.d/templates/errors-in-json-format.conf;
 }
diff --git a/roles/nginxplus/files/conf/http/templates/errors-in-json-format.conf b/roles/nginxplus/files/conf/http/templates/errors-in-json-format.conf
new file mode 100644
index 0000000000..ccc92069a0
--- /dev/null
+++ b/roles/nginxplus/files/conf/http/templates/errors-in-json-format.conf
@@ -0,0 +1,38 @@
+# This error handling template is intended for applications
+# like allsearch-api, which attempt to respond in json for
+# all requests
+#
+# The application creates descriptive JSON for 400 and 500
+# status codes, so those are not specifically handled here.
+#
+# More info at https://github.com/pulibrary/allsearch_api/blob/main/architecture-decisions/001_error_output.md
+
+error_page 401 402 404 405 406 407 408 409 411 412 413 414 415 416 417 418 421 422 423 424 426 428 431 451 501 502 503 504 505 506 507 508 510 511 /error.json;
+
+error_page 403 /forbidden.json;
+error_page 413 /too_large.json;
+error_page 429 /ratelimit.json;
+
+    location = /error.json {
+        ssi on;
+        internal;
+        root /var/local/www/default;
+    }
+
+    location = /forbidden.json {
+        ssi on;
+        internal;
+        root /var/local/www/default;
+    }
+
+    location = /too_large.json {
+        ssi on;
+        internal;
+        root /var/local/www/default;
+    }
+
+    location = /ratelimit.json {
+        ssi on;
+        internal;
+        root /var/local/www/default;
+    }
diff --git a/roles/nginxplus/files/error.json b/roles/nginxplus/files/error.json
new file mode 100644
index 0000000000..7b294b9415
--- /dev/null
+++ b/roles/nginxplus/files/error.json
@@ -0,0 +1,6 @@
+{
+    "error": {
+        "problem": "ERROR",
+        "message": "We encountered an error."
+    }
+}
diff --git a/roles/nginxplus/files/forbidden.json b/roles/nginxplus/files/forbidden.json
new file mode 100644
index 0000000000..09c66d40c8
--- /dev/null
+++ b/roles/nginxplus/files/forbidden.json
@@ -0,0 +1,6 @@
+{
+    "error": {
+        "problem": "FORBIDDEN",
+        "message": "You are not allowed to access this.  If you are attempting to reach a staging site, check if you are on VPN."
+    }
+}
diff --git a/roles/nginxplus/files/ratelimit.json b/roles/nginxplus/files/ratelimit.json
new file mode 100644
index 0000000000..696761ae3b
--- /dev/null
+++ b/roles/nginxplus/files/ratelimit.json
@@ -0,0 +1,6 @@
+{
+    "error": {
+        "problem": "TOO_MANY_REQUESTS",
+        "message": "You are making too many requests.  Please find a way to accomplish your task without making so many requests."
+    }
+}
diff --git a/roles/nginxplus/files/too_large.json b/roles/nginxplus/files/too_large.json
new file mode 100644
index 0000000000..ba3d462b40
--- /dev/null
+++ b/roles/nginxplus/files/too_large.json
@@ -0,0 +1,6 @@
+{
+    "error": {
+        "problem": "CONTENT_TOO_LARGE",
+        "message": "You are making a request that is too large for us to process.  If you are in a browser, check your cookies to make sure you are not sending many large cookies at once."
+    }
+}