diff --git a/web/src/billing/helpers.ts b/web/src/billing/helpers.ts
index f4c641c3e3..d3cccdc6de 100644
--- a/web/src/billing/helpers.ts
+++ b/web/src/billing/helpers.ts
@@ -80,7 +80,9 @@ export function create_ajax_request(
         },
         error(xhr) {
             $(form_loading).hide();
-            $(form_error).show().text(xhr.responseJSON.msg);
+            if (xhr.responseJSON?.msg) {
+                $(form_error).show().text(xhr.responseJSON.msg);
+            }
             $(form_input_section).show();
             $(zulip_limited_section).show();
             $(free_trial_alert_message).show();
diff --git a/web/src/channel.js b/web/src/channel.js
index 2024ed8e99..8cb3cfecc9 100644
--- a/web/src/channel.js
+++ b/web/src/channel.js
@@ -105,19 +105,16 @@ function call(args) {
                 return;
             }
         } else if (xhr.status === 403) {
-            try {
-                if (
-                    xhr.responseJSON.code === "CSRF_FAILED" &&
-                    reload_state.csrf_failed_handler !== undefined
-                ) {
-                    reload_state.csrf_failed_handler();
-                }
-            } catch (error) {
-                blueslip.error(
-                    "Unexpected 403 response from server",
-                    {xhr: xhr.responseText, args},
-                    error,
-                );
+            if (xhr.responseJSON === undefined) {
+                blueslip.error("Unexpected 403 response from server", {
+                    xhr: xhr.responseText,
+                    args,
+                });
+            } else if (
+                xhr.responseJSON.code === "CSRF_FAILED" &&
+                reload_state.csrf_failed_handler !== undefined
+            ) {
+                reload_state.csrf_failed_handler();
             }
         }
         orig_error(xhr, error_type, xhn);
@@ -189,7 +186,7 @@ export function patch(options) {
 }
 
 export function xhr_error_message(message, xhr) {
-    if (xhr.status.toString().charAt(0) === "4") {
+    if (xhr.status.toString().charAt(0) === "4" && xhr.responseJSON?.msg) {
         // Only display the error response for 4XX, where we've crafted
         // a nice response.
         const server_response_html = _.escape(xhr.responseJSON.msg);
diff --git a/web/src/compose.js b/web/src/compose.js
index a203df2472..9707af1a44 100644
--- a/web/src/compose.js
+++ b/web/src/compose.js
@@ -583,10 +583,14 @@ export function initialize() {
                 $invite_row.remove();
             }
 
-            function failure(error_msg) {
+            function xhr_failure(xhr) {
+                let error_message = "Failed to subscribe user!";
+                if (xhr.responseJSON?.msg) {
+                    error_message = xhr.responseJSON.msg;
+                }
                 clear_invites();
                 compose_banner.show_error_message(
-                    error_msg,
+                    error_message,
                     compose_banner.CLASSNAMES.generic_compose_error,
                     $banner_container,
                     $("#compose-textarea"),
@@ -594,11 +598,6 @@ export function initialize() {
                 $(event.target).prop("disabled", true);
             }
 
-            function xhr_failure(xhr) {
-                const error = xhr.responseJSON;
-                failure(error.msg);
-            }
-
             const sub = sub_store.get(stream_id);
 
             subscriber_api.add_user_ids_to_stream([user_id], sub, success, xhr_failure);
diff --git a/web/src/hotspots.js b/web/src/hotspots.js
index 489852e86e..1abd092021 100644
--- a/web/src/hotspots.js
+++ b/web/src/hotspots.js
@@ -66,10 +66,13 @@ export function post_hotspot_as_read(hotspot_name) {
         url: "/json/users/me/hotspots",
         data: {hotspot: hotspot_name},
         error(err) {
-            blueslip.error("Failed to fetch hotspots", {
-                status: err.status,
-                body: err.responseText,
-            });
+            if (err.readyState !== 0) {
+                blueslip.error("Failed to fetch hotspots", {
+                    readyState: err.readyState,
+                    status: err.status,
+                    body: err.responseText,
+                });
+            }
         },
     });
 }
diff --git a/web/src/invite.js b/web/src/invite.js
index 9c5048f041..4ad3289f92 100644
--- a/web/src/invite.js
+++ b/web/src/invite.js
@@ -114,7 +114,7 @@ function submit_invitation_form() {
             }
         },
         error(xhr) {
-            if (xhr.responseJSON.errors === undefined) {
+            if (xhr.responseJSON?.errors === undefined) {
                 // There was a fatal error, no partial processing occurred.
                 ui_report.error("", xhr, $invite_status);
             } else {
diff --git a/web/src/message_edit.js b/web/src/message_edit.js
index f74c3b62ec..b2df13d345 100644
--- a/web/src/message_edit.js
+++ b/web/src/message_edit.js
@@ -693,13 +693,15 @@ export function toggle_resolve_topic(message_id, old_topic_name, report_errors_i
         url: "/json/messages/" + message_id,
         data: request,
         error(xhr) {
-            if (xhr.responseJSON.code === "MOVE_MESSAGES_TIME_LIMIT_EXCEEDED") {
-                handle_resolve_topic_failure_due_to_time_limit(topic_is_resolved);
-                return;
-            }
+            if (xhr.responseJSON) {
+                if (xhr.responseJSON.code === "MOVE_MESSAGES_TIME_LIMIT_EXCEEDED") {
+                    handle_resolve_topic_failure_due_to_time_limit(topic_is_resolved);
+                    return;
+                }
 
-            if (report_errors_in_global_banner) {
-                ui_report.generic_embed_error(xhr.responseJSON.msg, 3500);
+                if (report_errors_in_global_banner) {
+                    ui_report.generic_embed_error(xhr.responseJSON.msg, 3500);
+                }
             }
         },
     });
@@ -842,7 +844,7 @@ export function save_inline_topic_edit($row) {
         },
         error(xhr) {
             const $spinner = $row.find(".topic_edit_spinner");
-            if (xhr.responseJSON.code === "MOVE_MESSAGES_TIME_LIMIT_EXCEEDED") {
+            if (xhr.responseJSON?.code === "MOVE_MESSAGES_TIME_LIMIT_EXCEEDED") {
                 const allowed_message_id = xhr.responseJSON.first_message_id_allowed_to_move;
                 const send_notification_to_old_thread = false;
                 const send_notification_to_new_thread = false;
@@ -1223,7 +1225,7 @@ export function move_topic_containing_message_to_stream(
         },
         error(xhr) {
             reset_modal_ui();
-            if (xhr.responseJSON.code === "MOVE_MESSAGES_TIME_LIMIT_EXCEEDED") {
+            if (xhr.responseJSON?.code === "MOVE_MESSAGES_TIME_LIMIT_EXCEEDED") {
                 const allowed_message_id = xhr.responseJSON.first_message_id_allowed_to_move;
                 function handle_confirm() {
                     move_topic_containing_message_to_stream(
diff --git a/web/src/portico/integrations.js b/web/src/portico/integrations.js
index 41b4ff07dc..74fc1bf357 100644
--- a/web/src/portico/integrations.js
+++ b/web/src/portico/integrations.js
@@ -196,11 +196,13 @@ function hide_catalog_show_integration() {
         dataType: "html",
         success: hide_catalog,
         error(err) {
-            blueslip.error(`Integration documentation for '${state.integration}' not found.`, {
-                readyState: err.readyState,
-                status: err.status,
-                responseText: err.responseText,
-            });
+            if (err.readyState !== 0) {
+                blueslip.error(`Integration documentation for '${state.integration}' not found.`, {
+                    readyState: err.readyState,
+                    status: err.status,
+                    responseText: err.responseText,
+                });
+            }
         },
     });
 }
diff --git a/web/src/portico/integrations_dev_panel.js b/web/src/portico/integrations_dev_panel.js
index 4e9684e0fd..8526cbb7c3 100644
--- a/web/src/portico/integrations_dev_panel.js
+++ b/web/src/portico/integrations_dev_panel.js
@@ -180,11 +180,10 @@ function update_url() {
 
 // API callers: These methods handle communicating with the Python backend API.
 function handle_unsuccessful_response(response) {
-    try {
+    if (response.responseJSON?.msg) {
         const status_code = response.statusCode().status;
-        response = JSON.parse(response.responseText);
-        set_results_notice(`Result: (${status_code}) ${response.msg}`, "warning");
-    } catch {
+        set_results_notice(`Result: (${status_code}) ${response.responseJSON.msg}`, "warning");
+    } else {
         // If the response is not a JSON response, then it is probably
         // Django returning an HTML response containing a stack trace
         // with useful debugging information regarding the backend
diff --git a/web/src/reactions.js b/web/src/reactions.js
index e3402949e4..256322a2cd 100644
--- a/web/src/reactions.js
+++ b/web/src/reactions.js
@@ -85,14 +85,16 @@ function update_ui_and_send_reaction_ajax(message_id, reaction_info) {
         },
         error(xhr) {
             view.waiting_for_server_request_ids.delete(reaction_request_id);
-            if (
-                xhr.responseJSON?.code === "REACTION_ALREADY_EXISTS" ||
-                xhr.responseJSON?.code === "REACTION_DOES_NOT_EXIST"
-            ) {
-                // Don't send error report for simple precondition failures caused by race
-                // conditions; the user already got what they wanted
-            } else {
-                blueslip.error(channel.xhr_error_message("Error sending reaction", xhr));
+            if (xhr.readyState !== 0) {
+                if (
+                    xhr.responseJSON?.code === "REACTION_ALREADY_EXISTS" ||
+                    xhr.responseJSON?.code === "REACTION_DOES_NOT_EXIST"
+                ) {
+                    // Don't send error report for simple precondition failures caused by race
+                    // conditions; the user already got what they wanted
+                } else {
+                    blueslip.error(channel.xhr_error_message("Error sending reaction", xhr));
+                }
             }
         },
     };
diff --git a/web/src/server_events.js b/web/src/server_events.js
index a9b8a29875..f1a58e09bf 100644
--- a/web/src/server_events.js
+++ b/web/src/server_events.js
@@ -207,7 +207,7 @@ function get_events({dont_block = false} = {}) {
                 get_events_xhr = undefined;
                 // If we're old enough that our message queue has been
                 // garbage collected, immediately reload.
-                if (xhr.status === 400 && xhr.responseJSON.code === "BAD_EVENT_QUEUE_ID") {
+                if (xhr.status === 400 && xhr.responseJSON?.code === "BAD_EVENT_QUEUE_ID") {
                     page_params.event_queue_expired = true;
                     reload.initiate({
                         immediate: true,
diff --git a/web/src/settings_account.js b/web/src/settings_account.js
index c36ae4c389..a5db61271f 100644
--- a/web/src/settings_account.js
+++ b/web/src/settings_account.js
@@ -118,9 +118,11 @@ function upload_avatar($file_input) {
             if (page_params.avatar_source === "G") {
                 $("#user-avatar-source").show();
             }
-            const $error = $("#user-avatar-upload-widget .image_file_input_error");
-            $error.text(xhr.responseJSON.msg);
-            $error.show();
+            if (xhr.responseJSON?.msg) {
+                const $error = $("#user-avatar-upload-widget .image_file_input_error");
+                $error.text(xhr.responseJSON.msg);
+                $error.show();
+            }
         },
     });
 }
@@ -490,7 +492,9 @@ export function set_up() {
                     $("#api_key_value").text(data.api_key);
                 },
                 error(xhr) {
-                    $("#user_api_key_error").text(xhr.responseJSON.msg).show();
+                    if (xhr.responseJSON?.msg) {
+                        $("#user_api_key_error").text(xhr.responseJSON.msg).show();
+                    }
                 },
             });
             e.preventDefault();
@@ -798,7 +802,7 @@ export function set_up() {
                         },
                     );
                     let rendered_error_msg;
-                    if (xhr.responseJSON.code === "CANNOT_DEACTIVATE_LAST_USER") {
+                    if (xhr.responseJSON?.code === "CANNOT_DEACTIVATE_LAST_USER") {
                         if (xhr.responseJSON.is_last_owner) {
                             rendered_error_msg = error_last_owner;
                         } else {
diff --git a/web/src/settings_bots.js b/web/src/settings_bots.js
index b6286e0745..fe58463ca7 100644
--- a/web/src/settings_bots.js
+++ b/web/src/settings_bots.js
@@ -580,8 +580,10 @@ export function set_up() {
                 $row.find("api_key_error").hide();
             },
             error(xhr) {
-                const $row = $(e.currentTarget).closest("li");
-                $row.find(".api_key_error").text(xhr.responseJSON.msg).show();
+                if (xhr.responseJSON?.msg) {
+                    const $row = $(e.currentTarget).closest("li");
+                    $row.find(".api_key_error").text(xhr.responseJSON.msg).show();
+                }
             },
         });
     });
diff --git a/web/src/settings_linkifiers.js b/web/src/settings_linkifiers.js
index 1c58a388ee..242cad2406 100644
--- a/web/src/settings_linkifiers.js
+++ b/web/src/settings_linkifiers.js
@@ -73,8 +73,7 @@ function open_linkifier_edit_form(linkifier_id) {
             },
             error_continuation(xhr) {
                 $change_linkifier_button.prop("disabled", false);
-                const response_text = xhr.responseJSON;
-                if (response_text.errors !== undefined) {
+                if (xhr.responseJSON?.errors) {
                     handle_linkifier_api_error(
                         xhr,
                         $pattern_status,
@@ -239,12 +238,14 @@ export function build_page() {
                 },
                 error(xhr) {
                     $add_linkifier_button.prop("disabled", false);
-                    handle_linkifier_api_error(
-                        xhr,
-                        $pattern_status,
-                        $template_status,
-                        $linkifier_status,
-                    );
+                    if (xhr.responseJSON?.errors) {
+                        handle_linkifier_api_error(
+                            xhr,
+                            $pattern_status,
+                            $template_status,
+                            $linkifier_status,
+                        );
+                    }
                 },
             });
         });
diff --git a/web/src/stats/stats.js b/web/src/stats/stats.js
index 579d453541..8b60d0555a 100644
--- a/web/src/stats/stats.js
+++ b/web/src/stats/stats.js
@@ -1101,7 +1101,9 @@ function get_chart_data(data, callback) {
             update_last_full_update(data.end_times);
         },
         error(xhr) {
-            $("#id_stats_errors").show().text(xhr.responseJSON.msg);
+            if (xhr.responseJSON?.msg) {
+                $("#id_stats_errors").show().text(xhr.responseJSON.msg);
+            }
         },
     });
 }
diff --git a/web/src/stream_create.js b/web/src/stream_create.js
index 5d9e636ce2..0efdb64eab 100644
--- a/web/src/stream_create.js
+++ b/web/src/stream_create.js
@@ -280,8 +280,7 @@ function create_stream() {
             // The rest of the work is done via the subscribe event we will get
         },
         error(xhr) {
-            const msg = xhr.responseJSON.msg;
-            if (msg.includes("access")) {
+            if (xhr.responseJSON?.msg?.includes("access")) {
                 // If we can't access the stream, we can safely
                 // assume it's a duplicate stream that we are not invited to.
                 //
diff --git a/web/src/stream_edit_subscribers.js b/web/src/stream_edit_subscribers.js
index 0b4d448588..7ce3b6bc52 100644
--- a/web/src/stream_edit_subscribers.js
+++ b/web/src/stream_edit_subscribers.js
@@ -196,9 +196,12 @@ function subscribe_new_users({pill_user_ids}) {
     }
 
     function invite_failure(xhr) {
-        const error = xhr.responseJSON;
+        let message = "Failed to subscribe user!";
+        if (xhr.responseJSON?.msg) {
+            message = xhr.responseJSON.msg;
+        }
         show_stream_subscription_request_result({
-            message: error.msg,
+            message,
             add_class: "text-error",
             remove_class: "text-success",
         });
diff --git a/web/src/typing.js b/web/src/typing.js
index da01b99944..c9f7a14ece 100644
--- a/web/src/typing.js
+++ b/web/src/typing.js
@@ -24,7 +24,9 @@ function send_typing_notification_ajax(user_ids_array, operation) {
         },
         success() {},
         error(xhr) {
-            blueslip.warn("Failed to send typing event: " + xhr.responseText);
+            if (xhr.readyState !== 0) {
+                blueslip.warn("Failed to send typing event: " + xhr.responseText);
+            }
         },
     });
 }
diff --git a/web/src/ui_report.ts b/web/src/ui_report.ts
index da21819833..a3e938768a 100644
--- a/web/src/ui_report.ts
+++ b/web/src/ui_report.ts
@@ -38,7 +38,7 @@ export function error(
     status_box: JQuery,
     remove_after?: number,
 ): void {
-    if (xhr && xhr.status >= 400 && xhr.status < 500) {
+    if (xhr && xhr.status >= 400 && xhr.status < 500 && xhr.responseJSON?.msg) {
         // Only display the error response for 4XX, where we've crafted
         // a nice response.
         const server_response_html = _.escape(xhr.responseJSON.msg);
@@ -78,7 +78,7 @@ export function generic_embed_error(error_html: string, remove_after: number): v
 }
 
 export function generic_row_button_error(xhr: JQuery.jqXHR, $btn: JQuery): void {
-    if (xhr.status >= 400 && xhr.status < 500) {
+    if (xhr.status >= 400 && xhr.status < 500 && xhr.responseJSON?.msg) {
         const $error = $("<p>").addClass("text-error").text(xhr.responseJSON.msg);
         $btn.closest("td").empty().append($error);
     } else {
diff --git a/web/src/unread_ops.js b/web/src/unread_ops.js
index ec979f34ca..b1d88e85f3 100644
--- a/web/src/unread_ops.js
+++ b/web/src/unread_ops.js
@@ -142,8 +142,10 @@ export function mark_all_as_read(args = {}) {
             dialog_widget.close_modal();
         },
         error(xhr) {
-            // If we hit the rate limit, just continue without showing any error.
-            if (xhr.responseJSON.code === "RATE_LIMIT_HIT") {
+            if (xhr.readyState === 0) {
+                // client cancelled the request
+            } else if (xhr.responseJSON?.code === "RATE_LIMIT_HIT") {
+                // If we hit the rate limit, just continue without showing any error.
                 const milliseconds_to_wait = 1000 * xhr.responseJSON["retry-after"];
                 setTimeout(() => mark_all_as_read(args), milliseconds_to_wait);
             } else {
@@ -241,8 +243,10 @@ export function mark_as_unread_from_here(
             }
         },
         error(xhr) {
-            // If we hit the rate limit, just continue without showing any error.
-            if (xhr.responseJSON.code === "RATE_LIMIT_HIT") {
+            if (xhr.readyState === 0) {
+                // client cancelled the request
+            } else if (xhr.responseJSON?.code === "RATE_LIMIT_HIT") {
+                // If we hit the rate limit, just continue without showing any error.
                 const milliseconds_to_wait = 1000 * xhr.responseJSON["retry-after"];
                 setTimeout(
                     () =>
diff --git a/web/src/user_group_edit_members.js b/web/src/user_group_edit_members.js
index 5b836f960a..9e52f9ddfc 100644
--- a/web/src/user_group_edit_members.js
+++ b/web/src/user_group_edit_members.js
@@ -223,9 +223,12 @@ function add_new_members({pill_user_ids}) {
     }
 
     function invite_failure(xhr) {
-        const error = xhr.responseJSON;
+        let message = "Failed to subscribe user!";
+        if (xhr.responseJSON?.msg) {
+            message = xhr.responseJSON.msg;
+        }
         show_user_group_membership_request_result({
-            message: error.msg,
+            message,
             add_class: "text-error",
             remove_class: "text-success",
         });
diff --git a/web/tests/reactions.test.js b/web/tests/reactions.test.js
index 1ebc54ae22..bdf54195df 100644
--- a/web/tests/reactions.test.js
+++ b/web/tests/reactions.test.js
@@ -268,7 +268,7 @@ test("sending", ({override, override_rewire}) => {
         // Since this path calls blueslip.warn, we need to handle it.
         blueslip.expect("error", "XHR error message.");
         channel.xhr_error_message = () => "XHR error message.";
-        args.error({responseJSON: {msg: "Some error message"}});
+        args.error({readyState: 4, responseJSON: {msg: "Some error message"}});
     }
     emoji_name = "alien"; // not set yet
     {